Allopolyploid Origin of Chenopodium album s. str. (Chenopodiaceae): A Molecular and Cytogenetic Insight
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27513342
PubMed Central
PMC4981418
DOI
10.1371/journal.pone.0161063
PII: PONE-D-16-01789
Knihovny.cz E-zdroje
- MeSH
- Chenopodium album genetika MeSH
- cytogenetické vyšetření metody MeSH
- DNA rostlinná genetika MeSH
- fylogeneze MeSH
- genetická variace genetika MeSH
- genomika MeSH
- molekulární evoluce * MeSH
- polyploidie * MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- DNA rostlinná MeSH
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.
Zobrazit více v PubMed
Rieseberg LH, Willis JH. Plant speciation. Science. 2007; 317: 910–914. PubMed PMC
Lowe AJ, Abbott RJ. Origins of the new allopolyploid species Senecio cambrensis (Asteraceae) and its relationship to the Canary Islands endemic Senecio teneriffae. Am J Bot. 1996; 83: 1365–1372.
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, Arachis hypogaea (Leguminosae). Am J Bot. 1996; 83: 1282–1291.
Cook LM, Soltis PS, Brunsfeld SJ, Soltis DE. Multiple independent formations of Tragopogon tetraploids (Asteraceae): evidence from RAPD markers. Mol Ecol. 1998; 7: 1293–1302.
Segraves KA, Thompson JN, Soltis PS, Soltis DE. Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia. Mol Ecol. 1999; 8: 253–262.
Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, et al. Towards resolving the Knautia arvensis agg. (Dipsacaceae) puzzle: primary and secondary contact zones and ploidy segregation at landscape and microgeographic scales. Ann Bot. 2009; 103: 963–974. 10.1093/aob/mcp016 PubMed DOI PMC
Mandák B, Trávníček P, Paštová L, Kořínková D. Is hybridization involved in the evolution of the Chenopodium album aggregate? An analysis based on chromosome counts and genome size estimation. Flora. 2012; 207: 530–540.
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 Reynoutria taxa in the Czech Republic. Ann Bot. 2003; 92: 265–272. PubMed PMC
Mandák B, Pyšek P, Bímová K. History of the invasion and distribution of Reynoutria taxa in the Czech Republic: a hybrid spreading faster than its parents. Preslia. 2004; 76: 15–64.
Mandák B, Bímová K, Pyšek P, Štěpánek J, Plačková I. Isoenzyme diversity in Reynoutria taxa: escape from sterility by hybridization. Plant Syst Evol. 2005; 253: 219–230.
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 Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Mol Ecol. 2009; 18: 4024–4048. 10.1111/j.1365-294X.2009.04329.x PubMed DOI
Symonds VV, Soltis PS, Soltis DE. Dynamics of polyploid formation in Tragopogon (Asteraceae): recurrent formation, gene flow, and population structure. Evolution. 2010; 64: 1984–2003. 10.1111/j.1558-5646.2010.00978.x PubMed DOI
Hunt HV, Ansell SW, Russell S, Schneider H, Vogel JC. Dynamics of polyploid formation and establishment in the allotetraploid rock fern Asplenium majoricum. Ann Bot. 2011; 108: 143–157. 10.1093/aob/mcr118 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 Arabis divaricarpa (Brassicaceae). Mol Biol Evol. 2003; 20: 338–350. PubMed
Zozomová-Lihová J, Krak K, Mandáková T, Shimizu KK, Španiel S, Vít P, et al. Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy. Ann Bot. 2014; 113: 817–830. 10.1093/aob/mcu012 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 Tragopogon castellanus (Asteraceae). New Phytol. 2015; 206: 1172–1183. 10.1111/nph.13227 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 Chenopodium: I. Chromosome number of Mexican tea (Ch. ambrosioides), American wormseed (Ch. ambrosioides L. var. anthelminticum A. Gray) and some allied species. Japanese Journal of Genetics. 1950; 25: 177–180.
Kawatani T, Ohno T. Chromosome numbers of genus Chenopodium. II. Japanes Journal of Genetics. 1956; 31: 15–17.
Giusti L. El gunero Chenopodium en Argentina. 1: Nomeros de cromosymas. Darwiniana. 1970; 16: 98–105.
Keener CS. Documented plant chromosome numbers 70:1. SIDA. 1970; 3: 533–536.
Uotila P. Chromosome counts on the Chenopodium album aggregate in Finland and NE Sweden. Ann Bot Fenn 1972; 9: 29–32.
Uotila P. Chromosome counts on Chenopodium L. from SE Europe and SW Asia. Ann Bot Fenn. 1973; 10: 337–340.
Palomino GH, Segura M, Bye R, Mercado PR. Cytogenetic distinction between Teloxys and Chenopodium (Chenopodiaceae). Southwest Nat. 1990; 35: 351–353.
Lomonosova MN, Krasnikov AA. Chromosome numbers in some species of genus Chenopodium (Chenopodiaceae) of the flora of Siberia. Bot Zhurn. 1994; 79: 124–125.
Lomonosova MN, Krasnikov AA. Chromosome numbers of the genus Chenopodium (Chenopodiaceae) in Siberia. Bot Zhurn. 2003; 88: 130–131.
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 Chenopodium (Chenopodiaceae). Genet Resour Crop Evol. 2006; 53: 1309–1320.
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 Chenopodium quinoa Willd. Genet Resour Crop Evol. 2015; 62, 913–925.
Walsh BM, Adhikary D, Maughan PJ, Emshwiller E, Jellen EN. Chenopodium polyploidy inferred from salt overly sensitive (SOS1) data. Am J Bot. 2015; 102: 533–543. 10.3732/ajb.1400344 PubMed DOI
Dvořák F. Study of Chenopodium interjectum J. Murr, Ch. mixtifolium J. Murr and Ch. laciniatum J. Murr. Feddes Repert. 1990; 101: 347–371.
Dvořák F. Study of Chenopodium purpurascens B. de Juss. ex Jacq. and on some related taxa. Feddes Repert. 1992; 103: 153–173.
Dvořák F. Study of Chenopodium subopulifolium J. Murr emend. D. Feddes Repert. 1992; 103: 49–69.
Dvořák F. Relationships and diagnostic characters of Chenopodium striatiforme J. Murr, C. striatum (Krašan) J. Murr and C. strictum Roth. Feddes Repert. 1993; 104: 439–449.
Dvořák F. Study of some species subsumed under Chenopodium probstii A. and on C. purpurascens B. de Juss. ex Jacq. Feddes Repert. 1994; 105: 113–139.
Jüttersonke B, Arlt K. Experimentelle Untersuchungen über die infraspezifische Struktur von Chenopodium album L. sowie Untersuchungen an Chenopodium suecicum J. Murr. Feddes Repert. 1989; 100: 1–63.
Uotila P. Chenopodium L In: Rechinger KH, editor. Flora Iranica, No. 172. Graz: Akademischen Druck und Verlagsanstalt; 1997. pp. 24–59.
Uotila P. Chenopodium L In: Jonsell B, editor. Flora Nordica 2. Stockholm: Royal Swedish Academy of Sciences; 2001. pp. 4–31.
Vít P, Krak K, Trávníček P, Douda J, Lomonosova MN, Mandák B. Genome size stability across Eurasian Chenopodium species (Amaranthaceae). Bot J Lin Soc. 2016; In press.
Gangopadhyay G, Das S, Mukherjee KK. Speciation in Chenopodium in West Bengal, India. Genet Resour Crop Evol. 2002; 49: 503–510.
Rahiminejad MR, Gornall RJ. Flavonoid evidence of allopolyploidy in the Chenopodium album aggregate (Amaranthaceae). Plant Syst Evol. 2004; 246: 77–87.
Fuentes-Bazan S, Mansion G, Borsch T. Towards a species level tree of the globally diverse genus Chenopodium (Chenopodiaceae). Mol Phylogenet Evol. 2012; 62: 359–374. 10.1016/j.ympev.2011.10.006 PubMed DOI
Fuentes-Bazan S, Uotila P, Borsch T. A novel phylogeny-based generic classification for Chenopodium sensu lato, and a tribal rearrangement of Chenopodioideae (Chenopodiaceae). Willdenowia. 2012; 42: 5–24.
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 Silene. Mol Biol Evol. 2003; 20: 1737–1740. 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 Arabidopsis thaliana. Plant J. 2001; 28: 689–697. 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 Triticeae species. Chromosome Res. 2001; 9: 129–136. PubMed
Mandák B, Krak K, Vít P, Pavlíková Z, Lomonosova MN, Habibi F, Douda J. How genome size variation is linked with evolution within Chenopodium sensu lato. Perspect. Plant Ecol. Evol. Syst. 2016. Submitted.
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 Triticum dicoccoides. Genome. 2000; 43: 1021–1026. 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 Chenopodium quinoa Willd. genome. Genome. 2011; 54: 710–717. 10.1139/G11-035 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 Tragopogon allopolyploids of recent and recurrent origin. Genetics. 2005; 169: 931–944. 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 Tragopogon (Asteraceae) allotetraploids. BMC Evol Biol. 2010; 10: 291 10.1186/1471-2148-10-291 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 Malus toringoides. Nord J Bot. 2015; 33: 109–119.
Queiroz CD, Batista FRD, de Oliveira LO. Evolution of the 5.8S nrDNA gene and internal transcribed spacers in Carapichea ipecacuanha (Rubiaceae) within a phylogeographic context. Mol Phylogenet Evol. 2011; 59: 293–302. 10.1016/j.ympev.2011.01.013 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 Achillea borealis (Asteraceae). Heredity. 2007; 98: 143–150. 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 Chenopodium suecicum and C. album in N Europe. Ann Bot Fenn. 1978; 108: 1–35.
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 Ranunculus auricomus complex. PlosOne. 2014; 9: e103003. PubMed PMC
Fuertes Aguilar J, Rossello JA, Nieto Feliner G. Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Mol Ecol. 1999; 8: 1341–1346. PubMed
Franzke A, Mummenhoff K. Recent hybrid speciation in Cardamine (Brassicaceae) -conversion of nuclear ribosomal ITS sequences in statu nascendi. Theor Appl Genet. 1999; 98: 831–834.
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 Cardamine × schulzii trigenomic allopolyploid. New Phytol. 2014; 203: 1096–1108. 10.1111/nph.12873 PubMed DOI
Kovařík A, Lim KY, Dadejová M, Matyášek R, Chase M, Knapp S, et al. Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot. 2008; 101: 815–823. 10.1093/aob/mcn019 PubMed DOI PMC
A pangenome reveals LTR repeat dynamics as a major driver of genome evolution in Chenopodium