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Phylogeography and allopolyploidization of Magnolia sect. Gynopodium (Magnoliaceae) in subtropical China

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Abstract

Magnolia sect. Gynopodium is an evergreen tree aggregate which includes five species exhibiting three different ploidy levels: diploid, tetraploid and hexaploid. These species have a broad distribution throughout subtropical China and extend to adjacent regions of Indochina. The chloroplast psbA-trnH sequences were used to examine the genetic structure and phylogeographical patterns for elucidating the glacial refugia and migration history of species within section Gynopodium, and the single-copy nuclear gene LEAFY sequences were cloned to retrieve the different distinct allelic sequences for inferring the polyploid origins. Seven chloroplast distinct haplotypes were identified for all the individuals within section Gynopodium. The ancestral haplotypes were confined to the eastern edge of Yun-Gui Plateau, Emei Mountain and the northwest Yunnan. All examined nuclear LEAFY allelic sequences were clustered into three distinct clades. Those of two diploid species were recovered as monophyletic and nested within the same clade, whereas those of the tetraploid and hexaploid species were placed into two and three different clades, respectively. The clear-cut geographical distributions of ancestral chloroplast haplotypes indicated multiple potential refugia for species within the section Gynopodium; the chloroplast haplotype distribution patterns suggested that these species experienced different migratory histories. The nuclear LEAFY phylogenetic pattern, combined with evidence from chloroplast data, showed that both allopatric differentiation and allopolyploid origin involving hybridization likely took part in the rapid evolution of the section Gynopodium.

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References

  • Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388. doi:10.2307/2405784

    Article  Google Scholar 

  • Azuma H, García-Franco JG, Rico-Gray V, Thien LB (2001) Molecular phylogeny of the Magnoliaceae: the biogeography of tropical and temperate disjunctions. Amer J Bot 88:2275–2285. doi:10.2307/3558389

    Article  CAS  Google Scholar 

  • Baack EJ, Stanton ML (2005) Ecological factors influencing tetraploid speciation in snow buttercups (Ranunculus adoneus): niche determination and tetraploid establishment. Evolution 59:1936–1944. doi:10.1554/05-168.1

    Article  PubMed  Google Scholar 

  • Chang KC (1989) The Neolithic Taiwan Strait. Kaogu 6:541–550,569

    Google Scholar 

  • Chen BL, Nooteboom HP (1993) Notes on Magnoliaceae III: the Magnoliaceae of China. Ann Missouri Bot Gard 80:999–1104. doi:10.2307/2399942

    Article  Google Scholar 

  • Chen RY, Chen ZG, Li XL, Song WQ (1985) Chromosome numbers of some species in the family Magnoliaceae in China. Acta Phytotax Sin 23:103–105

    Google Scholar 

  • Chen RY, Zhang W, Wu QA (1989) Chromosome numbers of some species in the family Magnoliaceae in Yunnan of China. Acta Bot Yunnan 11:234–238

    Google Scholar 

  • Chiang YC, Schaal BA (2006) Phylogeography of plants in Taiwan and the Ryukyu Archipelago. Taxon 55:3–41. doi:10.2307/25065526

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x

    Article  CAS  Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of chloroplast DNA and results for over 200 angiosperm species. Amer J Bot 75:1443–1458

    Article  Google Scholar 

  • Dong W, Liu J, Yu J, Wang L, Zhou S (2012) Highly variable chloroplast markers for evaluating plant phylogeny at low taxonomic levels and for DNA barcoding. PLoS ONE 7:e35071. doi:10.1371/journal.pone.0035071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ (1992) Gene trees and species trees: molecular systematics as one-character taxonomy. Syst Bot 17:144–163. doi:10.2307/2419070

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854. doi:10.1111/j.0014-3820.2000.tb01231.x

    CAS  PubMed  Google Scholar 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259. doi:10.1038/hdy.1994.35

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Figlar RB, Nooteboom HP (2004) Notes on Magnoliaceae IV. Blumea 49:87–100. doi:10.3767/000651904X486214

    Article  Google Scholar 

  • Frohlich MW, Parker DS (2000) The mostly male theory of flower evolutionary origins: from genes to fossils. Syst Bot 25:155–171. doi:10.2307/2666635

    Article  Google Scholar 

  • Gao LM, Moeller M, Zhang XM, Hollingsworth ML, Liu J, Mill RR, Gibby M, Li DZ (2007) High variation and strong phylogeographic pattern among cpDNA haplotypes in Taxus wallichiana (Taxaceae) in China and North Vietnam. Molec Ecol 16:4684–4698. doi:10.1111/j.1365-294X.2007.03537.x

    Article  CAS  Google Scholar 

  • Graur D, Li WH (1999) Fundamentals of molecular evolution. Sinauer & Associates, Sunderland

    Google Scholar 

  • Guo YP, Wang SZ, Vogl C, Ehrendorfer F (2012) Nuclear and plastid haplotypes suggest rapid diploid and polyploid speciation in the N Hemisphere Achillea millefolium complex (Asteraceae). BMC Evol Biol 12:2. doi:10.1186/1471-2148-12-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim S, Park CW, Kim YD, Suh Y (2001) Phylogenetic relationships in family Magnoliaceae inferred from ndhF sequences. Amer J Bot 88:717–728. doi:10.2307/2657073

    Article  CAS  Google Scholar 

  • Lee JY, Mummenhoff K, Bowman JL (2002) Allopolyploidization and evolution of species with reduced floral structures in Lepidium L. (Brassicaceae). Proc Natl Acad Sci USA 99:16835–16840. doi:10.1073/pnas.242415399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XL, Song WQ, An ZP, Chen RY (1998) Karyotype analysis of some species of Magnolia in China. Acta Bot Yunnan 20:204–206

    Google Scholar 

  • Liang H, Barakat A, Schlarbaum SE, Carlson JE (2011) Organization of the chromosome region harboring a FLORICAULA/LEAFY gene in Liriodendron. Tree Genet Genomes 7:373–384. doi:10.1007/s11295-010-0338-2

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Lin Q, Duan LD, Yuan Q, Li MH, Xie YH (2006) Taxonomic revision of the genus Parakmeria Huand Cheng (Magnoliaceae). Bull Bot Res Guangxi 27:527–531

    Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annual Rev Ecol Evol Syst 27:237–277. doi:10.1146/annurev.ecolsys.27.1.237

    Article  Google Scholar 

  • Meng AP, Wang HC, Li JQ, Sima YK (2006) A karyomorphological study of 40 species in 11 genera of the Magnoliaceae from China. Acta Phytotax Sin 44:47–63. doi:10.1360/aps040092

    Article  Google Scholar 

  • Miller JS, Venable DL (2000) Polyploidy and the evolution of gender dimorphism in plants. Science 289:2335–2338

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nie ZL, Wen J, Azuma H, Qiu YL, Sun H, Meng Y, Sun WB, Zimmer EA (2008) Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear data sets. Molec Phylogen Evol 48:1027–1040. doi:10.1016/j.ympev.2008.06.004

    Article  CAS  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploidy incidence and evolution. Annual Rev Genet 34:401–437. doi:10.1016/j.ympev.2008.06.004

    Article  CAS  Google Scholar 

  • Parris JK, Ranney TG, Knap HT, Baird WV (2010) Ploidy levels, relative genome sizes, and base pair composition in Magnolia. J Amer Soc Hort Sci 135:533–547

    Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45. doi:10.1016/S0169-5347(00)02026-7

    Article  CAS  PubMed  Google Scholar 

  • Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in temperate plant species diversity. Nature 407:180–182. doi:10.1038/35025052

    Article  CAS  PubMed  Google Scholar 

  • Qiu YX, Fu CX, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Molec Phylogen Evol 59:225–244. doi:10.1016/j.ympev.2011.01.012

    Article  Google Scholar 

  • Ramsey J, Robertson A, Husband B (2008) Rapid adaptive divergence in New World Achillea, an autopolyploid complex of ecological races. Evolution 62:639–653

    Article  CAS  PubMed  Google Scholar 

  • Sang T (2002) Utility of low-copy nuclear gene sequences in plant phylogenetics. Crit Rev Biochem Molec Biol 37:121–147. doi:10.1080/10409230290771474

    Article  CAS  Google Scholar 

  • Shi S, Jin H, Zhong Y, He X, Huang Y, Tan F, Boufford DE (2000) Phylogenetic relationships of the Magnoliaceae inferred from chloroplast DNA matK sequences. Theor Appl Genet 101:925–930. doi:10.1007/s001220051563

    Article  CAS  Google Scholar 

  • Shi MM, Michalski SG, Welk E, Chen XY, Durka W (2014) Phylogeography of a widespread Asian subtropical tree: genetic east–west differentiation and climate envelope modelling suggest multiple glacial refugia. J Biogeogr 41:1710–1720. doi:10.1111/jbi.12322

    Article  Google Scholar 

  • Small RL, Cronn RC, Wendel JF (2004) L.A.S. Johnson review, 2: use of nuclear genes for phylogeny reconstruction in plants. Austral Syst Bot 17:145–170. doi:10.1071/SB03015

    Article  CAS  Google Scholar 

  • Sun X, Chen Y (1991) Palynological records of the last 11,000 yr in China. Quaternary Sci Rev 10:537–545

    Article  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109

    Article  CAS  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molec Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vu QN, Xia NH (2011) A new combination of Parakmeria (Magnoliaceae) from Vietnam. J Trop Subtrop Bot 19:313–316. doi:10.3969/j.issn.1005-3395.2011.04.003

    Google Scholar 

  • Wang WT (1992) On some distribution patterns and some migration routes found in the eastern Asiatic region. Acta Phytotax Sin 30:1–24

    CAS  Google Scholar 

  • Wang HS, Zhang YL (1994) The biodiversity and characters of spermatophytic genera endemic to China. Acta Bot Yunnan 16:209–220

    Google Scholar 

  • Wang YL, Li Y, Zhang SZ, YU XS (2006) The utility of matK gene in the phylogenetic analysis of the genus Magnolia. Acta Phytotax Sin 44:135–147. doi:10.1360/aps040013

    Article  Google Scholar 

  • Wang J, Gao P, Kang M, Lowe AJ, Huang H (2009) Refugia within refugia: the case study of a canopy tree (Eurycorymbus cavaleriei) in subtropical China. J Biogeogr 36:2156–2164. doi:10.1111/j.1365-2699.2009.02165.x

    Article  Google Scholar 

  • Wu CY (1965) On the tropical affinities of Chinese flora. Chin Sci Bull 10:25–33

    Google Scholar 

  • Xia N, Liu Y, Nooteboom HP. 2008. Magnoliaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 7. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, pp 48–91

  • Yan HF, Zhang CY, Wang FY, Hu CM, Ge XJ, Hao G (2012) Population expanding with the phalanx model and lineage split by environmental heterogeneity: a case study of Primula obconica in subtropical China. PLoS ONE 7:e41315. doi:10.1371/journal.pone.0041315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu G, Chen X, Ni J, Cheddadi R, Guiot J, Han H, Harrison SP et al (2000) Palaeovegetation of China: a pollen databased synthesis for the mid-Holocene and last glacial maximum. J Biogeogr 27:635–664. doi:10.1046/j.1365-2699.2000.00431.x

    Article  Google Scholar 

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Acknowledgements

Thank Tsai-Wen Hsu for collecting the materials of M. kachirachirai from Taiwan, Alison Wee and Jessie Han for their valuable comments and discussions on an earlier version of the manuscript. This research was supported by grants from the National Natural Science Foundation of China (Grant No. 31070209), the project of Botany Key Construction Disciplines of Hunan, and the Doctoral Scientific Foundation of Southwest Forestry University (Grant No. 111441).

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Correspondence to Long-Qian Xiao.

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Handling editor: Yunpeng Zhao.

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606_2017_1409_MOESM1_ESM.pdf

Online Resource 1. Summary of the chloroplast trnH–psbA sequence variation among seven haplotypes observed in section Gynopodium (PDF 25 kb)

Online Resource 2. The alignment matrix of the psbA-trnH sequences (PDF 34 kb)

The alignment matrix of the LEAFY sequences (PDF 93 kb)

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Information on Electronic Supplementary Material

Online Resource 1 . Summary of the chloroplast psbA-trnH sequence variation among seven haplotypes observed in section Gynopodium.

Online Resource 2 . The alignment matrix of the psbA-trnH sequences.

Online Resource 3 . The alignment matrix of the LEAFY sequences.

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Xiao, LQ., Li, QQ. Phylogeography and allopolyploidization of Magnolia sect. Gynopodium (Magnoliaceae) in subtropical China. Plant Syst Evol 303, 957–967 (2017). https://doi.org/10.1007/s00606-017-1409-8

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