The study of hybridization processes within genus Sparganium L. Subgenus Xanthosparganium holmb. Based on data of next generation sequencing (NGS)

Cover Page

Cite item

Abstract

The study represents the results of research of intragenic polymorphism in transcribed spacer ITS1 of the 35S rRNA genes in representatives of subgenus Xanthosparganium genus Sparganium which were obtained by means of locus-specific next generation sequencing on the platform Illumina MiSeq. It was shown that ribotype variations in studied samples generally correspond to the division of this genus into three sections – Erecta (subgenus Sparganium), Natantia and Minima (subgenus Xanthosparganium). High level of intragenic polymorphism was revealed in S. hyperboreum, with ribotypes distributed among several groups. Genome of this species includes ribotypes which are typical for other species in subgenus Xanthosparganium. For two investigated S. glomeratum samples, there were no ribotypes similar to such ribotypes in other species of Natantia section. S. glomeratum has got ribotypes identical with S. hyperboreum of Minima section. This feature may be the evidence of ancient intersectional hybridization of these two species. Characteristics of rDNA in S. glomeratum are in favor of putting this species into Minima section. It was suggested that speciation processes within the genus could be based not only on hybridization but also went on in allopatric way. The fist statement is supported by the presence of similar and identical ribotypes in S. emersum, S. × longifolium, S. gramineum and S. hyperboreum, the second – as it was mentioned by other researchers, is due to close relationship between North American and Eurasian taxa.

About the authors

Evgeniy A. Belyakov

Papanin Institute for Biology of Inland Waters, RAS; Cherepovets State University

Email: eugenybeliakov@yandex.ru
SPIN-code: 6944-1980

Candidate of Biological Sciences, Senior Researcher, Laboratory of Higher Aquatic Plants

Russian Federation, 109, Borok, Nekouz, Yaroslavl, 152742; 5, Lunacharscy street, Cherepovets, 162600

Eduard M. Machs

Komarov Botanical Institute RAS

Email: emachs@binran.ru
SPIN-code: 9496-0538
Scopus Author ID: 8619012500
ResearcherId: J-4970-2018

Candidate of Biological Sciences, Senior Researcher, Laboratory of Biosystematics and Cytology

Russian Federation, 2, Professor Popov str., Saint Petersburg, 197376

Yulia V. Mikhailova

Komarov Botanical Institute RAS

Email: ymikhaylova@binran.ru
ORCID iD: 0000-0001-9278-0937
SPIN-code: 4271-1072
Scopus Author ID: 6506004774
ResearcherId: L-7482-2015

Candidate of Biological Sciences, Researcher, Laboratory of Biosystematics and Cytology

Russian Federation, 2, Professor Popov str., Saint Petersburg, 197376

Aleksandr V. Rodionov

Komarov Botanical Institute RAS; St. Petersburg State University

Author for correspondence.
Email: avrodionov@mail.ru
ORCID iD: 0000-0003-1146-1622
SPIN-code: 6206-2123
Scopus Author ID: 23767636100

Doctor of Biological Sciences, Professor, Chief Researcher with the Assignment of the Duties of the Head of the Laboratory of Biosystematics and Cytology

Russian Federation, 2, Professor Popov str., Saint Petersburg, 197376; 7/9, Universitetskaya embankment, Saint-Petersburg, 199034

References

  1. Baack EJ, Rieseberg LH. A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev. 2007;17(6):513-518. https://doi.org/10.1016/j.gde.2007.09.001.
  2. Soltis PS, Soltis DE. The role of hybridization in plant speciation. Annu Rev Plant Biol. 2009;60:561-588. https://doi.org/10.1146/annurev.arplant.043008.092039.
  3. Носов Н.Н., Пунина Е.О., Мачс Э.М., Родионов А.В. Межвидовая гибридизация в происхождении видов растений на примере рода Poa sensu lato // Успехи современной биологии. – 2015. – Т. 135. – № 1. – С. 21–39. [Nosov NN, Punina EO, Machs EM, Rodionov AV. Interspecies hybridization in the origin of plant species: cases in the genus Poa sensu lato. Biology Bulletin Reviews. 2015;5(4):366-382.] https://doi.org/10.1134/S2079086415040088.
  4. Родионов А.В., Амосова А.В., Беляков Е.А., и др. Генетические последствия межвидовой гибридизации, ее роль в видообразовании и фенотипическом разнообразии растений // Генетика. – 2019. – Т. 55. – № 3. – С. 255–272. https://doi.org/10.1134/S0016675819030159. [Rodionov AV, Amosova AV, Belyakov EA, et al. Genetic consequences of interspecific hybridization, its role in speciation and phenotypic diversity of plants. Russian Journal of Genetics. 2019;55(3): 278-294.] doi: 10.1134/S1022795419030141.
  5. Whitney KD, Ahern JR, Campbell LG, et al. Patterns of hybridization in plants. Perspect Plant Ecol Evol Syst. 2010;12(3):175-182. https://doi.org/10.1016/j.ppees.2010.02.002.
  6. Kaplan Z, Fehrer J. Molecular identification of hybrids from a former hot spot of Potamogeton hybrid diversity. Aquat Bot. 2013;105:34-40. https://doi.org/10.1016/j.aquabot.2012.11.002.
  7. Iida S, Kadono Y, Kosuge K. Maternal effects and ecological divergence in aquatic plants: a case study in natural reciprocal hybrids between Potamogeton perfoliatus and P. wrightii. Plant Species Biol. 2013;28(1):3-11. https://doi.org/10.1111/1442-1984.12006.
  8. Ito Y, Tanaka N, Pooma R, Tanaka N. DNA barcoding reveals a new record of Potamogeton distinctus (Potamogetonaceae) and its natural hybrids, P. distinctus × P. nodosus and P. distinctus × P. wrightii (P. malainoides) from Myanmar. Biodivers Data J. 2014;2: e1073. https://doi.org/10.3897/bdj.2.e1073.
  9. Yang T, Zhang TI, Guo YH, Liu X. Identification of hybrids in Potamogeton: incongruence between plastid and its regions solved by a novel barcoding marker PHYB. PLoS ONE. 2016;11(11):1-12. https://doi.org/10.1371/journal.pone.0166177.
  10. Arrigo N, Bétrisey S, Graf L, et al. Hybridization as a threat in climate relict Nuphar pumila (Nymphaeaceae). Biodivers Conserv. 2016;25(10):1863-1877. https://doi.org/10.1007/s10531-016-1165-z.
  11. Borsch T, Wiersema JH, Hellquist CB, et al. Speciation in North American water lilies: evidence for the hybrid origin of the newly discovered Canadian endemic Nymphaea loriana sp. nov. (Nymphaeaceae) in a past contact zone. Botany. 2014;92(12):867-882. https://doi.org/10.1139/cjb-2014-0060.
  12. Nierbauer KU, Kanz B, Zizka G. The widespread naturalisation of Nymphaea hybrids is masking the decline of wild-type Nymphaea alba in Hesse, Germany. Flora. 2014;209(2):122-130. https://doi.org/10.1016/j.flora.2013.12.005.
  13. Wiecław H, Koopman J. Numerical analysis of morphology of natural hybrids between Carex hostiana and the members of Carex flava agg. (Cyperaceae). Nord J Bot. 2013;31(4):464-472. https://doi.org/10.1111/j.1756-1051.2013.00095.x.
  14. Więcław H, Wilhelm M. Natural hybridization within the Carex flava complex (Cyperaceae) in Poland: morphometric studies. Ann Bot Fenn. 2014;51(3):129-147. https://doi.org/10.5735/085.053.0101.
  15. Pedersen AT, Nowak MD, Brysting AK, et al. Correction: hybrid origins of Carex rostrate var. borealis and C. stenolepis, two problematic taxa in Carex section Vesicariae (Cyperaceae). PLoS ONE. 2016;11(10): 1-18. https://doi.org/10.1371%2Fjournal.pone.0165430.
  16. Zalewska-Gałosz J, Jopek M, Ilnicki T. Hybridization in Batrachium group: controversial delimitation between heterophyllous Ranunculus penicillatus and the hybrid Ranunculus fluitans × R. peltatus. Aquat Bot. 2015;120:160-168. https://doi.org/10.1016/j.aquabot.2014.03.002.
  17. Bobrov AA, Zalewska-Gałosz J, Jopek M, Movergoz EA. Ranunculus schmalhausenii (section Batrachium, Ranunculaceae), a neglected water crowfoot endemic to Fennoscandia – a case of rapid hybrid speciation in postglacial environment of North Europe. Phytotaxa. 2015;233(2):101-138. https://doi.org/10.11646/ phytotaxa.233.2.1.
  18. Ball D, Freeland J. Synchronous flowering times and asymmetrical hybridization in Typha latifolia and T. angustifolia in northeastern North America. Aquat Bot. 2013;104:224-227. https://doi.org/10.1016/j.aquabot.2012.08.006.
  19. Freeland J, Ciotir C, Kirk H. Regional differences in the abundance of native, introduced, and hybrid Typha spp. in northeastern North America influence wetland invasions. Biol Invasions. 2013;15(12):2651-65. https://doi.org/10.1007/s10530-013-0481-4.
  20. Givnish TJ, Barfuss MH, van Ee B, et al. Phylogeny, adaptive radiation, and historical biogeography in Bromaliaceae: insights from an 8-locus plastid phylogeny. Am J Bot. 2011;98(5):872-895. https://doi.org/10.3732/ajb.1000059.
  21. Givnish TJ, Zuluaga A, Spalink D, et al. Monocot plastid phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. Am J Bot. 2018;105(11): 1888-1910. https://doi.org/10.1002/ajb2.1178.
  22. Sulman JD, Drew BT, Drummond C, et al. Systematics, biogeography, and character evolution of Sparganium (Typhaceae): diversification of a widespread, aquatic lineage. Am J Bot. 2013;100(10):2023-2039. https://doi.org/10.3732/ajb.1300048.
  23. Ito Y, Tanaka N, Kim C, et al. Phylogeny of Sparganium (Typhaceae) revisited: non-monophyletic nature of S. emersum sensu lato and resurrection of S. acaule. Plant Syst Evol. 2016;302(1):129-135. https://doi.org/10.1007/s00606-015-1245-7.
  24. Su T, Yang JX, Lin YG, et al. Characterization of the complete chloroplast genome of Sparganium stoloniferum (Poales: Typhaceae) and phylogenetic analysis. Mitochondrial DNA B Resour. 2019;4(1):1402-1403. https://doi.org/10.1080/23802359.2019.1598798.
  25. Leitch IJ, Johnston E, Pellicer J, et al. Plant DNA C-values database. Release 7.1, April 2019. Available from: https://cvalues.science.kew.org/.
  26. Родионов А.В., Ким Е.С., Пунина Е.О., и др. Эволюция хромосомных чисел в трибах Aveneae и Poeae по данным сравнительного исследования внутренних транскрибируемых спейсеров ITS1 и ITS2 ядерных генов 45S рРНК // Ботанический журнал. – 2007. – Т. 92. – № 1. – С. 57–71. [Rodionov AV, Kim ES, Punina EO, et al. Evolution of chromosome numbers in the tribes Aveneae and Poeae inferred from the comparative analysis of the internal transcribed spacers ITS1 and ITS2 of nuclear 45S rRNA genes. Botanicheskii zhurnal. 2007;92(1):57-71. (In Russ.)]
  27. Salse J. Deciphering the evolutionary interplay between subgenomes following polyploidy: a paleogenomics approach in grasses. Am J Bot. 2016;103(7):1167-1174. https://doi.org/10.3732/ajb.1500459.
  28. Болховских З.В., Гриф В.Г., Захарьева О.И., Матвеева Т.С. Хромосомные числа цветковых растений. – Л.: Наука, 1969. – 926 с. [Bolkhovskikh ZV, Grif VG, Zakharyeva OI, Matveeva TS. Khromosomnyye chisla tsvetkovykh rasteniy. Leningrad: Nauka; 1969. 926 p. (In Russ.)]
  29. Агапова Н.Д., Архарова К.Б., Вахтина Л.И., и др. Числа хромосом цветковых растений флоры СССР: Moraceae-Zygophyllaceae. – СПб.: Наука, 1993. – 427 с. [Agapova ND, Arkharova KB, Vakhtina LI, et al. Chisla khromosom tsvetkovykh rasteniy flory SSSR: Moraceae-Zygophyllaceae. Saint Petersburg: Nauka; 1993. 427 p. (In Russ.)]
  30. Kim CS, Kim SY, Meon MO. A new record for the Korean flora: Sparganium fallax Graebn. (Sparganiaceae). Korean J Plant Taxonomy. 2010;40(3):169-173. https://doi.org/10.11110/kjpt.2010.40.3.169.
  31. Goldblatt P. Polyploidy in angiosperms: monocotyledons. In: Polyploidy. Boston (MA): Springer; 1980. рр. 219-239.
  32. Anderson E. Introgressive hybridization. London–New York: Hafner Publ. Co.; 1969. 109 p.
  33. Seitz U, Seitz U. Molecular-weight of ribosomal-RNA precursor molecules and their processing in higher-plant cells. Z Naturforsch C Biosci. 1979;34(3-4): 253-258. https://doi.org/10.1515/znc-1979-3-416.
  34. Garcia S, Kovařík A, Leitch AR, Garnatje T. Cytogenetic features of rRNA genes across land plants: analysis of the plant rDNA database. Plant J. 2017;89(5):1020-1030. https://doi.org/10.1111/tpj.13442.
  35. Родионов А.В., Гнутиков A.А., Коцинян А.Р., и др. Последовательность ITS1-5.8S рДНК-ITS2 в генах 35S рРНК как маркер при реконструкции филогении злаков (сем. Poaceae) // Уcпехи современной биологии. – 2016. – Т. 136. – № 5. – С. 419–437. [Rodionov AV, Gnutikov AA, Kotsinyan AR, et al. ITS1-5.8S rDNA-ITS2 sequence in 35S rRNA genes as marker for reconstruction of phylogeny of grasses (Poaceae family). Biology Bulletin Reviews, 2017, 7(2):85-102. (In Russ.)]. https://doi.org/10.1134/S2079086417020062.
  36. Egan AN, Schlueter J, Spooner DM. Applications of next-generation sequencing in plant biology. Am J Bot. 2012;99(2):175-185. https://doi.org/10.3732/ajb.1200020.
  37. Пунина Е.О., Мачс Э.М., Крапивская Е.Е., Родионов А.В. Полиморфные сайты в транскрибируемых спейсерах генов 35Sр РНК пионов как индикатор происхождения сортов // Генетика. – 2017. – Т. 53. – № 2. – С. 181-191. [Punina EO, Machs EM, Krapivskaya EE, Rodionov AV. Pilymorphic sites in transcribed spacers of 35S rRNA genes as an indicator of origin of the Paeonia cultivars. Russian Journal of Genetics. 2017;53(2):202-212.] https://doi.org/10.1134/S1022795417010112.
  38. Пунина Е.О., Мачс Э.М., Крапивская Е.Е., и др. Межвидовая гибридизация в роде Paeonia (Paeoniaceae): полиморфные сайты в транскрибируемых спейсерах генов 45S рРНК как индикаторы происхождения природных и искусственных гибридов пионов // Генетика. – 2012. – Т. 48. – № 7. – С. 812. [Punina EO, Machs EM, Krapivskaya EE, et al. Interspecific hybridization in the genus Paeonia (Paeoniaceae): polymorphic sites in transcribed spacers of the 45S rRNA genes as indicators of natural and artificial peony hybrids. Russian Journal of Genetics. 2012;48(7):684-697.] https://doi.org/10.1134/S1022795412070113.
  39. Андронова Е.В., Мачс Е.М., Филиппов Е.Г., и др. Филогеография таксонов рода Cyprepedium (Orchidaceae) на территории России // Ботанический журнал. – 2017. – Т. 102. – № 8. – С. 1027-1059. [Andronova EV, Machs EM, Filippov EG, et al. Phylogeography of the Genus Cyprepedium (Orchidaceae) taxa in Russia. Botanicheskii zhurnal. 2017;102(8): 1027-1059. (In Russ.)]. https://doi.org/10.1134/S0006813617080014.
  40. Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin. 1987;19(1):11-15.
  41. National Center for Biotechnology Information. GenBank Overview. Available from: https://www.ncbi.nlm.nih.gov/genbank/.
  42. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-2120. https://doi.org/10.1093/bioinformatics/btu170.
  43. Aronesty E. Сomparison of sequencing utility program. Open Bioinformatics J. 2013;7:1-8. https://doi.org/10.2174/1875036201307010001.
  44. Taylor SA, Larson EL, Harrison RG. Hybrid zones: windows on climate change. Trends Ecol Evol. 2015;30(7):398-406. https://doi.org/10.1016/j.tree.2015.04.010.
  45. Vallejo-Marin M, Hiscock SJ. Hybridization and hybrid speciation under global change. New Phytologist. 2016;211(4):1170-1187. https://doi.org/10.1111/nph.14004.
  46. Preston CD, Pearman DA. Plant hybrids in the wild: evidence from biological recording. Biol J Linn Soc Lond. 2015;115(3):555-572. https://doi.org/10.1111/bij.12577.
  47. Дорофеев П.И. Третичные флоры Западной Сибири. – М., Л.: Издательство Академии наук СССР, 1963. – 346 с. [Dorofeev PI. Tretichnyye flory Zapadnoy Sibiri. Moscow-Leningrad: Izdatel’stvo Akademii Nauk SSSR; 1963. 346 p. (In Russ.)]
  48. Дорофеев П.И. К систематике третичных Sparganium // Советская палеокарпология: итоги и перспективы / Сб. статей под ред. Г.И. Горецкого, В.П. Гричук. – М.: Наука, 1979. – С. 53–75. [Dorofeev PI. K sistematike tretichnykh Sparganium. In: (Collected papers) Sovetskaya paleokarpologiya: itogi i perspektivy. Ed. by G.I. Goretskiy, V.P. Grichuk. Moscow: Nauka; 1979. рр. 53-75. (In Russ.)]
  49. Беляков Е.А., Щербаков А.В., Лапиров А.Г., Шилов М.П. Морфология и экологические особенности Sparganium × longifolium (Typhaceae) в центре Европейской части России // Biosystems Diversity. – 2017. – Vol. 25. – № 2. – P. 154–161. [Belyakov EA, Shcherbakov AV, Lapirov AG, Shilov MP. Morphology and ecological characteristics of Sparganium × longifolium (Typhaceae) in the Central part of European Russia. Biosystems Diversity. 2017;25(2):154-161. (In Russ.)]. https://doi.org/10.15421/011723.
  50. Виноградова Ю.К., Галкина М.А. Гибридизация как фактор инвазионной активности чужеродных видов золотарника (Solidago) // Журнал общей биологии. – 2019. – Т. 80. – № 1. – С. 43–56. [Vinogradova YuK, Galkina MA. Hybridization as a factor of invasive activity of alien species of goldenrods (Solidago). Journal of general biology. 2019;80(1):43-56. (In Russ.)]. https://doi.org/10.1134/S004445961901007X.
  51. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10(3):512-526. https://doi.org/10.1093/oxfordjournals.molbev.a040023.
  52. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870-1874. https://doi.org/10.1093/molbev/msw054.
  53. Цвелев Н.Н. Заметки о некоторых гидрофильных растениях флоры СССР // Новости систематики высших растений. – 1984. – Т. 21. – С. 232–242. [Tzvelev NN. Notulae de florae URSS plants hydrophilis nonnulis. Novitates systematicae plantarum vascularium. 1984;21:232-242. (In Russ.)]
  54. Cook CD, Nicholls MS. A monographic study of the genus Sparganium. Part 2: Subgenus Sparganium. Bot Helv. 1987;97(1):1-44.
  55. Снакин В.В. Динамика биоразнообразия, дрейф материков и глобализация // Век глобализации. – 2015. – № 1. – С. 66–74. [Snakin VV. The Dynamics of biodiversity, continental drift and globalization. Age of Globalization. 2015;(1):66-74. (In Russ.)]
  56. Chaw SM, Zharkikh A, Sung HM, et al. Molecular phylogeny of extant gymnosperms and seed plant evolution: analysis of nuclear 18S rRNA sequences. Mol Biol Evol. 1997;14(1):56-68. https://doi.org/10.1093/oxfordjournals.molbev.a025702.

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. Molecular phylogenetic analysis and ITS1 ribotypes within the genus Sparganium of the subgenus Xanthosparganium, according to the NGS. Molecular phylogenetic analysis was conducted applying the maximum likelihood method, based on the Tamura–Ney model [51]. The tree with the highest logarithmic probability is presented (-1211.06). The percentage of trees in which related taxa are grouped together is presented at the branch nodes. Source trees for heuristic searches were obtained based on the Neighbor–Join and BioNJ algorithms, according to the pairwise distance matrix, which is estimated by the maximum composite likelihood with the subsequent selection of the topology with the highest value of logarithmic probability. A tree was created to scale, and the length of the branches was measured by the number of substitutions per site. The analysis used 56 nucleotide sequences. In total, there were 339 positions in the final data set. An evolutionary analysis was conducted at MEGA7 [52]. The first letter (A–F) in the name of the ribotype corresponds to a decrease in the frequency of occurrence (A is the highest)

Download (178KB)

Copyright (c) 2019 Belyakov E., Machs E., Mikhailova Y., Rodionov A.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies