What nature separated, and human joined together: About a spontaneous hybridization between two allopatric dogwood species (Cornus controversa and C. alternifolia)


Autoři: Barbara Gawrońska aff001;  Maria Morozowska aff002;  Katarzyna Nuc aff001;  Piotr Kosiński aff002;  Ryszard Słomski aff001
Působiště autorů: Department of Biochemistry and Biotechnology, Faculty of Agronomy and Bioengineering, Poznań University of Life Sciences, Dojazd, Poznań, Poland aff001;  Department of Botany, Faculty of Horticulture and Landscape Architecture, Poznań University of Life Sciences, Wojska Polskiego, Poznań, Poland aff002;  Institute of Dendrology, Polish Academy of Sciences, Parkowa, Kórnik, Poland aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226985

Souhrn

In this study, possible hybridization between two allopatric species, Cornus controversa and Cornus alternifolia, was explored using molecular and morphological approaches. Scanning electron microscope analyses of the adaxial and the abaxial leaf surfaces yielded a few new not yet described characters typical for the particular species and intermediate for hybrids. With the use of 14 Random Amplified Polymorphic DNA and 5 Amplified Fragment Length Polymorphism primer combinations, 44 fragments species specific to C. controversa and 51 species specific to C. alternifolia were obtained. Most of these bands were also found in putative hybrids. All clustering analyses based on binary data combined from both methods confirmed a separate and intermediate status of the hybrids. Hybrid index estimates for hybrids C1-C5 indicated that all were the first generation of offspring (F1). Chloroplast intergenic spacers (trnF-trnL and psbC-trnS) were used to infer the hybridization direction. Based on the assumption of maternal inheritance of chloroplast DNA, C. controversa seems to be the maternal parent of the hybrid. Internal transcribed spacer sequences of the five hybrids analyzed here indicated higher similarity with the sequences of C. controversa (all shared the majority of its single nucleotide polymorphisms). Sequence analysis of PI-like genes fully confirmed the hybrid origin of C1-C5 hybrids. Our results also showed that two specimens in the C. alternifolia group, A1 and A3, are not free of introgression. They are probably repeated backcrosses toward C. alternifolia. Furthermore, molecular data seem to point not only to unidirectional introgression toward C. controversa (the presence of hybrids) but to bidirectional introgression as well, since the presence of markers specific for C. controversa in the profiles of C. alternifolia specimen A3 was observed.

Klíčová slova:

Amplified fragment length polymorphism – Hybridization – Introgression – Leaves – Polymerase chain reaction – Random amplified polymorphic DNA technique – Trichomes – Abaxial surface


Zdroje

1. Gross BL, Rieseberg LH. The Ecological Genetics of Homoploid Hybrid Speciation. J Hered. 2005;96: 241–252. doi: 10.1093/jhered/esi026 15618301

2. Mallet J. Hybrid speciation. Nature. 2007;446: 279–283. doi: 10.1038/nature05706 17361174

3. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, et al. Polyploidy and angiosperm diversification. Am J Bot. 2009;96: 336–348. doi: 10.3732/ajb.0800079 21628192

4. Harrison RG, Larson EL. Hybridization, Introgression, and the Nature of Species Boundaries. J Hered. 2014;105: 795–809. doi: 10.1093/jhered/esu033 25149255

5. Anderson E. Introgressive hybridization. New York: J. Wiley & Sons; 1949.

6. Whitney KD, Randell RA, Rieseberg LH. Adaptive Introgression of Herbivore Resistance Traits in the Weedy Sunflower Helianthus annuus. Am Nat. 2006;167: 794–807. doi: 10.1086/504606 16649157

7. Nachman MW, Payseur BA. Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice. Philos Trans R Soc B. 2012;367: 409–421. doi: 10.1098/rstb.2011.0249 22201170

8. Pardo-Diaz C, Salazar C, Baxter SW, Merot C, Figueiredo-Ready W, Joron M, et al. Adaptive Introgression across Species Boundaries in Heliconius Butterflies. PLOS Genetics. 2012;8: e1002752. doi: 10.1371/journal.pgen.1002752 22737081

9. Teeter KC, Thibodeau LM, Gompert Z, Buerkle CA, Nachman MW, Tucker PK. The Variable Genomic Architecture of Isolation Between Hybridizing Species of House Mice. Evolution. 2010;64: 472–485. doi: 10.1111/j.1558-5646.2009.00846.x 19796152

10. Cinget B, Lafontaine G de, Gérardi S, Bousquet J. Integrating phylogeography and paleoecology to investigate the origin and dynamics of hybrid zones: insights from two widespread North American firs. Mol Ecol. 2015;24: 2856–2870. doi: 10.1111/mec.13194 25865063

11. Currat M, Ruedi M, Petit RJ, Excoffier L. The Hidden Side of Invasions: Massive Introgression by Local Genes. Evolution. 2008;62: 1908–1920. doi: 10.1111/j.1558-5646.2008.00413.x 18452573

12. Stebbins GL. The Role of Hybridization in Evolution. Proc Am Philos Soc. 1959;103: 231–251.

13. Grant V. Plant Speciation. New York: University Presses of California, Columbia and Princeton; 1981.

14. Abbott RJ. Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol. 1992;7: 401–405. doi: 10.1016/0169-5347(92)90020-C 21236080

15. Arnold ML. Natural Hybridization and Evolution. New York: Oxford University Press; 1997.

16. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, et al. Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization. Science. 2003;301: 1211–1216. doi: 10.1126/science.1086949 12907807

17. Soltis DE, Soltis PS, Rieseberg DLH. Molecular Data and the Dynamic Nature of Polyploidy. CRC Crit Rev Plant Sci. 1993;12: 243–273. doi: 10.1080/07352689309701903

18. Cronn R, Wendel JF. Cryptic trysts, genomic mergers, and plant speciation. New Phytol. 2004;161: 133–142. doi: 10.1111/j.1469-8137.2004.00947.x

19. Rieseberg LH. Hybrid Origins of Plant Species. Annu Rev Ecol Syst. 1997;28: 359–389. doi: 10.1146/annurev.ecolsys.28.1.359

20. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC. Homoploid Hybrid Speciation in an Extreme Habitat. Science. 2006;314: 1923–1925. doi: 10.1126/science.1135875 17138866

21. Nagamitsu T, Kawahara T, Kanazashi A. Endemic dwarf birch Betula apoiensis (Betulaceae) is a hybrid that originated from Betula ermanii and Betula ovalifolia. Plant Species Biol. 2006;21: 19–29. doi: 10.1111/j.1442-1984.2006.00147.x

22. Feliner GN, Álvarez I, Fuertes-Aguilar J, Heuertz M, Marques I, Moharrek F, et al. Is homoploid hybrid speciation that rare? An empiricist’s view. Heredity. 2017;118: 513–516. doi: 10.1038/hdy.2017.7 28295029

23. Hegarty MJ, Hiscock SJ. Hybrid speciation in plants: new insights from molecular studies. New Phytol. 2005;165: 411–423. doi: 10.1111/j.1469-8137.2004.01253.x 15720652

24. Schumer M, Rosenthal GG, Andolfatto P. How Common Is Homoploid Hybrid Speciation? Evolution. 2014;68: 1553–1560. doi: 10.1111/evo.12399 24620775

25. Eyde RH. ComprehendingCornus: Puzzles and progress in the systematics of the dogwoods. Bot Rev. 1988;54: 233–351. doi: 10.1007/BF02868985

26. Xiang Q-Y, Boufford DE. Cornaceae. In: Wu ZY, Raven PH, Hong DY, editors. Flora of China. Beijing: Science Press; 2005. pp. 206–221.

27. Schulz B. Die Gattung Cornus (Cornaceae), Hartriegel und Kornelkirsche, Teile 1 und 2. Teil 1: Übersicht über die Gattung. Teil 2: Die Wechselständigen Hartriegel Cornus alternifolia L.f. 1782 und Cornus controversa Hemsley 1909. Mitt Deutsch Dendrol Gesel. 2011; 67–83.

28. Schulz B. Die Gattung Cornus (Cornaceae), Hartriegel und Kornelkirsche. Teil 3: Die kleinfrüchtigen Hartriegel (Untergattung Kraniopsis). Mitt Deutsch Dendrol Gesel. 2012; 91–132.

29. Murrell ZE. Phylogenetic Relationships in Cornus (Cornaceae). Syst Bot. 1993;18: 469–495. doi: 10.2307/2419420

30. Fan C, Xiang (Jenny) Qiu-Yun. Phylogenetic relationships within Cornus (Cornaceae) based on 26S rDNA sequences. Am J Bot. 2001;88: 1131–1138. doi: 10.2307/2657096 11410478

31. Fan C, Xiang Q-Y (Jenny). Phylogenetic analyses of Cornales based on 26S rRNA and combined 26S rDNA-MATK-RBCL sequence data. Am J Bot. 2003;90: 1357–1372. doi: 10.3732/ajb.90.9.1357 21659236

32. Xiang Q-Y (Jenny), Thorne JL, Seo T-K, Zhang W, Thomas DT, Ricklefs RE. Rates of nucleotide substitution in Cornaceae (Cornales)—Pattern of variation and underlying causal factors. Mol Phylogenet Evol. 2008;49: 327–342. doi: 10.1016/j.ympev.2008.07.010 18682295

33. Xiang Q-Y (Jenny), Thomas DT, Zhang W, Manchester SR, Murrell Z. Species level phylogeny of the genus Cornus (Cornaceae) based on molecular and morphological evidence—implications for taxonomy and Tertiary intercontinental migration. TAXON. 2006;55: 9–30. doi: 10.2307/25065525

34. Feng C-M, Xiang Q-Y (Jenny), Franks RG. Phylogeny-based developmental analyses illuminate evolution of inflorescence architectures in dogwoods (Cornus s. l., Cornaceae). New Phytol. 2011;191: 850–869. doi: 10.1111/j.1469-8137.2011.03716.x 21488878

35. Wadl PA, Skinner JA, Dunlap JR, Reed SM, Rinehart TA, Pantalone VR, et al. Honeybee-mediated Controlled Pollinations in Cornus florida and C. kousa Intra- and Interspecific Crosses. HortScience. 2009;44: 1527–1533.

36. Rehder A. A new hybrid Cornus (Cornus rugosa × stolonifera). Rhodora. 1910;12: 121–124.

37. Kehne CL. The Case of the Dunbar Dogwood: A Neglected Hybrid. Arnoldia. 1978;38: 50–54.

38. Wagner WH. A natural hybrid of gray dogwood, Cornus racemosa, and round-leaved dogwood, C. rugosa, from Michigan. Mich Bot. 1990;29: 131–137.

39. Clay SN, Nath J. Cytogenetics of Some Species of Cornus. Cytologia. 1971;36: 716–730. doi: 10.1508/cytologia.36.716

40. Rehder A. Manual of cultivated trees and shrubs hardy in North America: exclusive of the subtropical and warmer temperate regions. 2nd ed. New York: Macmillan; 1967.

41. Hardin JW, Murrell ZE. Foliar Micromorphology of Cornus. J Torrey Bot Soc. 1997;124: 124–139. doi: 10.2307/2996580

42. Woźnicka A, Melosik I, Morozowska M. Quantitative and qualitative differences in morphological traits of endocarps revealed between Cornus L. species. Plant Syst Evol. 2015;301: 291–308. doi: 10.1007/s00606-014-1073-1

43. Li H-L. Floristic Relationships between Eastern Asia and Eastern North America. Trans Am Philos Soc. 1952;42: 371–429. doi: 10.2307/1005654

44. Boufford DE, Spongberg SA. Eastern Asian-Eastern North American Phytogeographical Relationships-A History From the Time of Linnaeus to the Twentieth Century. Ann Mo Bot Gard. 70: 423.

45. Xiang Q-Y, Brunsfeld SJ, Soltis DE, Soltis PS. Phylogenetic Relationships in Cornus Based on Chloroplast DNA Restriction Sites: Implications for Biogeography and Character Evolution. Syst Bot. 1996;21: 515–534. doi: 10.2307/2419612

46. Liao P-C, Shih H-C, Yen T-B, Lu S-Y, Cheng Y-P, Chiang Y-C. Molecular evaluation of interspecific hybrids between Acer albopurpurascens and A. buergerianum var. formosanum. Bot Stud. 2010;51: 8.

47. Morozowska M, Gawrońska B, Woźnicka A. Morphological, anatomical and genetic differentiation of Cornus mas, Cornus officinalis and their interspecific hybrid. Dendrobiology. 2013;70: 45–57.

48. Lee NS, Yeau SH, Park JO, Roh MS. Molecular evidence for hybridization ofIlex x wandoensis (Aquifoliaceae) by RAPD analysis. J Plant Biol. 2006;49: 491–497. doi: 10.1007/BF03031131

49. Smith NR, Trigiano RN, Windham MT, Lamour KH, Finley LS, Wang X, et al. AFLP Markers Identify Cornus florida Cultivars and Lines. J Am Soc Hortic Sci. 2007;132: 90–96. doi: 10.21273/JASHS.132.1.90

50. Feliner GN, Rosselló JA. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. ‎Mol Phylogenetics Evol. 2007;44: 911–919. doi: 10.1016/j.ympev.2007.01.013 17383902

51. Sang T. Utility of Low-Copy Nuclear Gene Sequences in Plant Phylogenetics. Crit Rev Biochem Mol Biol. 2002;37: 121–147. doi: 10.1080/10409230290771474 12139440

52. Small RL, Cronn RC, Wendel JF. Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot. 2004;17: 145. doi: 10.1071/SB03015

53. Álvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenetics Evol. 2003;29: 417–434. doi: 10.1016/S1055-7903(03)00208-2

54. Jack T. Plant development going MADS. Plant Mol Biol. 2001;46: 515–520. doi: 10.1023/a:1010689126632 11516144

55. Theißen G, Melzer R, Rümpler F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development. 2016;143: 3259–3271. doi: 10.1242/dev.134080 27624831

56. Zhang W, Xiang Q-Y (Jenny), Thomas DT, Wiegmann BM, Frohlich MW, Soltis DE. Molecular evolution of PISTILLATA-like genes in the dogwood genus Cornus (Cornaceae). Mol Phylogenet Evol. 2008;47: 175–195. doi: 10.1016/j.ympev.2007.12.022 18304837

57. Stellari GM, Jaramillo MA, Kramer EM. Evolution of the APETALA3 and PISTILLATA Lineages of MADS-Box–Containing Genes in the Basal Angiosperms. Mol Biol Evol. 2004;21: 506–519. doi: 10.1093/molbev/msh044 14694075

58. Epidermal Barthlott W. and seed surface characters of plants: systematic applicability and some evolutionary aspects. Nord J Bot. 1981;1: 345–355. doi: 10.1111/j.1756-1051.1981.tb00704.x

59. Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, et al. Classification and terminology of plant epicuticular waxes. Bot J Linn Soc. 1998;126: 237–260. doi: 10.1111/j.1095-8339.1998.tb02529.x

60. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 1990;18: 6531–6535. doi: 10.1093/nar/18.22.6531 1979162

61. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995;23: 4407–4414. doi: 10.1093/nar/23.21.4407 7501463

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

63. Delaporte KL, Collins GG, Conran JG, Sedgley M. Molecular analysis of an interspecific hybrid ornamental eucalypt for parental identification. Euphytica. 2001;122: 165–170. doi: 10.1023/A:1012619314419

64. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, et al. The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313: 1596–1604. doi: 10.1126/science.1128691 16973872

65. Culpepper JH, Sayavedra-Soto LA, Bassam BJ, Gresshoff PM. Characterization of Cornus (Dogwood) Genotypes Using DNA Fingerprinting. J Am Soc Hortic Sci. 1991;116: 1103–1107. doi: 10.21273/JASHS.116.6.1103

66. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23: 254–267. doi: 10.1093/molbev/msj030 16221896

67. Bryant D, Moulton V. Neighbor-Net: An agglomerative method for the construction of phylogenetic networks. Mol Biol Evol. 2004;21: 255–265. doi: 10.1093/molbev/msh018 14660700

68. Hammer O, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001;4: Unpaginated.

69. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155: 945–959. 10835412

70. Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. 2007;7: 574–578. doi: 10.1111/j.1471-8286.2007.01758.x 18784791

71. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour. 2015;15: 1179–1191. doi: 10.1111/1755-0998.12387 25684545

72. 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 15969739

73. Earl DA, von Holdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4: 359–361. doi: 10.1007/s12686-011-9548-7

74. Fritz RS, Nichols-Orians CM, Brunsfeld SJ. Interspecific Hybridization of Plants and Resistance to Herbivores: Hypotheses, Genetics, and Variable Responses in a Diverse Herbivore Community. Oecologia. 1994;97: 106–117. doi: 10.1007/BF00317914 28313595

75. Gompert Z, Buerkle CA. INTROGRESS: a software package for mapping components of isolation in hybrids. Mol Ecol Resour. 2010;10: 378–384. doi: 10.1111/j.1755-0998.2009.02733.x 21565033

76. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018. Available: http://www.R-project.org/

77. Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol. 1991;17: 1105–1109. doi: 10.1007/bf00037152 1932684

78. Demesure B, Sodzi N, Petit RJ. A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol. 1995;4: 129–134. doi: 10.1111/j.1365-294x.1995.tb00201.x 7711952

79. White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: A Guide to Methods and Applications. San Diego: Academic Press; 1990. pp. 315–322. doi: 10.1016/B978-0-12-372180-8.50042–1

80. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. PNAS. 1988;85: 2444–2448. doi: 10.1073/pnas.85.8.2444 3162770

81. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22: 4673–4680. doi: 10.1093/nar/22.22.4673 7984417

82. Meirmans PG. Seven common mistakes in population genetics and how to avoid them. Mol Ecol. 2015;24: 3223–3231. doi: 10.1111/mec.13243 25974103

83. Kim C, Deng T, Wen J, Nie Z-L, Sun H. Systematics, biogeography, and character evolution of Deutzia (Hydrangeaceae) inferred from nuclear and chloroplast DNA sequences. Mol Phylogenet Evol. 2015;87: 91–104. doi: 10.1016/j.ympev.2015.03.002 25776523

84. Ellstrand NC, Whitkus R, Rieseberg LH. Distribution of spontaneous plant hybrids. PNAS. 1996;93: 5090–5093. doi: 10.1073/pnas.93.10.5090 11607681

85. Whitney KD, Ahern JR, Campbell LG, Albert LP, King MS. Patterns of hybridization in plants. Perspect Plant Ecol Syst. 2010;12: 175–182. doi: 10.1016/j.ppees.2010.02.002

86. Mameli G, López-Alvarado J, Farris E, Susanna A, Filigheddu R, Garcia-Jacas N. The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae). Bot J Linn Soc. 2014;175: 453–467. doi: 10.1111/boj.12177

87. Aas G. Taxonomical impact of morphological variation in Quercus robur and Q. petraea: a contribution to the hybrid controversy. Ann For Sci. 1993;50: 107s–113s. doi: 10.1051/forest:19930709

88. Curtu AL, Gailing O, Finkeldey R. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evol Biol. 2007;7: 218. doi: 10.1186/1471-2148-7-218 17996115

89. Orton ER. Interspecific hybridization among Cornus florida, C. kousa, and C. nutallii. Proc Intl Plant Prop Soc. 1985;35: 655–650.

90. Ament MH, Windham MT, Trigiano RN. Determination of parentage of flowering dogwood (Cornus florida) seedlings using DNA amplification fingerprinting. J Arboric. 2000;26: 206–212.

91. Reed SM. Self-incompatibility in Cornus florida. HortScience. 2004;39: 335–338. doi: 10.21273/HORTSCI.39.2.335

92. Tomaszewski D, Zieliński J. Epicuticular wax structures on stems and comparison between stems and leaves–A survey. Flora. 2014;209: 215–232. doi: 10.1016/j.flora.2014.03.001

93. Zieliński J, Tomaszewski T, Gawlak M, Orlova L. Kłopotliwe derenie—Cornus alba L. i C. sericea L. (Cornaceae). Dwa gatunki czy jeden? [Troublesome dogwoods–Cornus alba L. and C. sericea L. (Cornaceae). Two species or one?]. Rocznik PTD. 2014;62: 9–23.

94. Soltis DE, Mavrodiev EV, Doyle JJ, Rauscher J, Soltis PS. ITS and ETS Sequence Data and Phylogeny Reconstruction in Allopolyploids and Hybrids. Syst Bot. 2008;33: 7–20. doi: 10.1600/036364408783887401

95. Darnell JE, Lodish HF, Baltimore D. Molecular Cell Biology. 2nd edition. New York: Scientific Amer Inc; 1990.

96. Huckett BI, Botha FC. Stability and potential use of RAPD markers in a sugarcane genealogy. Euphytica. 1995;86: 117–125. doi: 10.1007/BF00022017

97. Ayliffe MA, Lawrence GJ, Ellis JG, Pryor AJ. Heteroduplex molecules formed between allelic sequences cause nonparental RAPD bands. Nucleic Acids Res. 1994;22: 1632–1636. doi: 10.1093/nar/22.9.1632 8202363

98. Zhao X, Zhang J, Zhang Z, Wang Y, Xie W. Hybrid identification and genetic variation of Elymus sibiricus hybrid populations using EST-SSR markers. Hereditas. 2017;154: 1–15. doi: 10.1186/s41065-016-0023-z

99. Kirk H, Máčel M, Klinkhamer PGL, Vrieling K. Natural hybridization between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence. Mol Ecol. 2004;13: 2267–2274. doi: 10.1111/j.1365-294X.2004.02235.x 15245400

100. Schwarzbach AE, Rieseberg LH. Likely multiple origins of a diploid hybrid sunflower species. Mol Ecol. 2002;11: 1703–1715. doi: 10.1046/j.1365-294x.2002.01557.x 12207721

101. Rieseberg L, Wendel J. lntrogression and Its Consequences in Plants. In: Harrison RG, editor. Hybrid Zones and the Evolutionary Process. Oxford: Oxford University Press; 1993. pp. 70–109.

102. Barker MS, Rieseberg LH. Evolutionary genomics of hybridization: Detecting ancient hybridization and introgression by the inference of intrologs in plant genomes. University of British Columbia; 2008. Available: http://2008.botanyconference.org/engine/search/index.php?func=detail&aid=706

103. Álvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol. 2003;29: 417–434. doi: 10.1016/s1055-7903(03)00208-2 14615184

104. Bailey CD, Carr TG, Harris SA, Hughes CE. Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol. 2003;29: 435–455. doi: 10.1016/j.ympev.2003.08.021 14615185

105. Emshwiller E, Doyle J. Origins of domestication and polyploidy in oca (Oxalis tuberosa: Oxalidaceae): nrDNA ITS data. Am J Bot. 1998;85: 975. 21684981

106. 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. doi: 10.1007/s001220051140

107. Hodkinson TR, Chase MW, Lledó DM, Salamin N, Renvoize SA. Phylogenetics of Miscanthus, Saccharum and related genera (Saccharinae, Andropogoneae, Poaceae) based on DNA sequences from ITS nuclear ribosomal DNA and plastid trnL intron and trnL-F intergenic spacers. J Plant Res. 2002;115: 381–392. doi: 10.1007/s10265-002-0049-3 12579363

108. Yang T, Zhang T, Guo Y, Liu X. Identification of Hybrids in Potamogeton: Incongruence between Plastid and ITS Regions Solved by a Novel Barcoding Marker PHYB. PLOS ONE. 2016;11: e0166177. doi: 10.1371/journal.pone.0166177 27855191

109. Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ. The its Region of Nuclear Ribosomal DNA: A Valuable Source of Evidence on Angiosperm Phylogeny. Ann Missouri Bot Gard. 1995;82: 247–277. doi: 10.2307/2399880

110. Aguilar JF, Rosselló JA, Feliner GN. Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Mol Ecol. 1999;8: 1341–1346. doi: 10.1046/j.1365-294x.1999.00690.x 10447874

111. Wendel JF, Schnabel A, Seelanan T. An Unusual Ribosomal DNA Sequence from Gossypium gossypioides Reveals Ancient, Cryptic, Intergenomic Introgression. Mol Phylogenetics Evol. 1995;4: 298–313. doi: 10.1006/mpev.1995.1027 8845966


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