Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

Genome differentiation, natural hybridisation and taxonomic relationships among Eleocharis viridans, E. niederleinii and E. ramboana (Cyperaceae)

Carlos Roberto Maximiano da Silva A , Thaíssa Boldieri de Souza A , Rafael Trevisan B , María Socorro González-Elizondo C , José Marcelo Domingues Torezan D , Rogério Fernandes de Souza A and André Luís Laforga Vanzela A E
+ Author Affiliations
- Author Affiliations

A Laboratory of Cytogenetics and Plant Diversity, Department of General Biology, Center for Biological Sciences, State University of Londrina, Londrina, 86051-970, PR, Brazil.

B Department of Botany, Federal University of Santa Catarina, Florianópolis, 88010-970, SC, Brazil.

C CIIDIR, Instituto Politécnico Nacional, Sigma Fraccionamiento 20 de Noviembre II, 34220 Durango, Durango, Mexico.

D Laboratory of Biodiversity and Ecosystem Restoration, State University of Londrina, 86051-970, PR, Brazil.

E Corresponding author. Email: andrevanzela@uel.br

Australian Systematic Botany 30(2) 183-195 https://doi.org/10.1071/SB17002
Submitted: 5 January 2017  Accepted: 26 May 2017   Published: 17 August 2017

Abstract

The role of natural hybridisation and genome changes in the differentiation and speciation of Eleocharis (Cyperaceae) was addressed through the study of the following three closely related species of the polyphyletic series Tenuissimae: Eleocharis viridans Kük. ex Osten, E. ramboana R.Trevis & Boldrini and E. niederleinii Boech., which often reproduce asexually. Molecular and cytogenetic data were used to understand the genomic and karyotypic relationships in the group. Genomes were compared using internal transcribed spacer–cleaved amplified polymorphic sequence (ITS-CAPS) marker and confirmed with random amplified polymorphic DNA, which allowed identification of different genetic groups, with clear evidence of natural hybrids. Karyotype analysis showed numerical variation from 2n = 20–42, with occurrence of chromosome heteromorphisms and polymorphisms, including variability in 35S rDNA site numbers. Meiotic studies demonstrated irregular pairing in some samples, which is associated with hybridisation and asexual reproduction. Genomic in situ hybridisation (GISH) reactions were conducted using two well defined genetic groups as probes, with 2n = 20 and normal meiosis. Probes were tested against each one of the genetic groups and showed positive, partial and negative GISH results, which supported the molecular analysis data. The results indicated that the three studied species are undergoing an intense process of genomic and karyotypic re-arrangement, which results in overlapping of morphological and genomic characteristics. The present study has exemplified the value of an integrative taxonomic approach to solve conflicts in species delimitation in groups undergoing hybridisation.

Additional keywords: dysploidy, GISH, hybrids, molecular markers, polyploidy, symploidy, series Tenuissimae, 35S rDNA.


References

Alves MV, Araújo AC, Prata AP, Vitta FA, Hefler SM, Trevisan R, Gil AB, Martins S, Thomas SWW (2010) Diversity of Cyperaceae in Brazil. Rodriguésia 60, 1–12.

Arguelho EG, Michelan VS, Nogueira FM, da Silva CRM, Rodriguez C, Trevisan R, Vanzela ALL (2012) New chromosome counts in Brazilian species of Rhynchospora (Cyperaceae). Caryologia 65, 140–146.
New chromosome counts in Brazilian species of Rhynchospora (Cyperaceae).CrossRef |

Bureš P (1998) A high polyploidy Eleocharis uniglumis S.L. (Cyperaceae) from central and southeastern Europe. Folia Geobotanica 33, 429–439.
A high polyploidy Eleocharis uniglumis S.L. (Cyperaceae) from central and southeastern Europe.CrossRef |

Bureš P, Rotreklová O, Stoneberg HSD, Pikner R (2004) Cytogeographical survey of Eleocharis subser. Eleocharis in Europe 1. Eleocharis palustris. Folia Geobotanica 39, 235–257.
Cytogeographical survey of Eleocharis subser. Eleocharis in Europe 1. Eleocharis palustris.CrossRef |

Catling PM (1994) Eleocharis compressa × Eleocharis erythropoda, a new natural hybrid spike rush from Ontario. Canadian Journal of Botany 72, 837–842.
Eleocharis compressa × Eleocharis erythropoda, a new natural hybrid spike rush from Ontario.CrossRef |

Catling PM, Reznicek AA, Denford K (1989) Carex lacustris × C. trichocarpa (Cyperaceae), a new natural hybrid. Canadian Journal of Botany 67, 790–795.
Carex lacustris × C. trichocarpa (Cyperaceae), a new natural hybrid.CrossRef |

Chase MW, Knapp S, Cox AV, Clarrson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS (2003) Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Annals of Botany 92, 107–127.
Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae).CrossRef | 1:CAS:528:DC%2BD3sXmtVKqtL0%3D&md5=c7312a26f973c11bfb47ca0864138c21CAS |

da Silva CRM, González-Elizondo MS, Vanzela ALL (2005) Reduction of chromosome number in Eleocharis subarticulata (Cyperaceae) by multiple translocations. Botanical Journal of the Linnean Society 149, 457–464.
Reduction of chromosome number in Eleocharis subarticulata (Cyperaceae) by multiple translocations.CrossRef |

da Silva CRM, González-Elizondo MS, Vanzela ALL (2008a) Chromosome reduction in Eleocharis maculosa (Cyperaceae). Cytogenetic and Genome Research 122, 175–180.
Chromosome reduction in Eleocharis maculosa (Cyperaceae).CrossRef | 1:STN:280:DC%2BD1M%2FktFSgug%3D%3D&md5=27bbe3aec053285adde235cfecb4898fCAS |

da Silva CRM, González-Elizondo MS, Rego LNAA, Torezan JMD, Vanzela ALL (2008b) Cytogenetical and cytotaxonomical analysis of some Brazilian species of Eleocharis. Australian Journal of Botany 56, 82–90.
Cytogenetical and cytotaxonomical analysis of some Brazilian species of Eleocharis.CrossRef |

da Silva CRM, Trevisan R, González-Elizondo MS, Ferreira JM, Vanzela ALL (2010a) Karyotypic diversification and its contribution to the taxonomy of Eleocharis (Cyperaceae) from Brazil. Australian Journal of Botany 58, 49–60.
Karyotypic diversification and its contribution to the taxonomy of Eleocharis (Cyperaceae) from Brazil.CrossRef |

da Silva CRM, Quintas CC, Vanzela ALL (2010b) Distribution of 45S and 5S rDNA sites in 23 species of Eleocharis (Cyperaceae). Genetica 138, 951–957.
Distribution of 45S and 5S rDNA sites in 23 species of Eleocharis (Cyperaceae).CrossRef | 1:CAS:528:DC%2BC3cXht1eltL7L&md5=54340945d1424987f8c9f1a53d6fa8a3CAS |

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

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.

Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574–578.
Inference of population structure using multilocus genotype data: dominant markers and null alleles.CrossRef | 1:CAS:528:DC%2BD2sXpslOhtbc%3D&md5=d20f78614f2ecaefb5ed0a28addc2a7fCAS |

Fay MF, Cowan RS, Simpson DA (2003) Hybridization between Schoenoplectus tabernaemontani and S. triqueter (Cyperaceae) species in the British Isles. Watsonia 24, 433–442.

Friesen N, Fritsch R, Bachmann K (1997) Hybrid origin of some ornamentals of Allium subgenus Melanocrommyum verified with GISH and RAPD. Theoretical and Applied Genetics 95, 1229–1238.
Hybrid origin of some ornamentals of Allium subgenus Melanocrommyum verified with GISH and RAPD.CrossRef | 1:CAS:528:DyaK1cXnvVemsA%3D%3D&md5=b015c09a37dca29a26c92a24092b3018CAS |

Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Research 7, 1869–1885.
Cloning and characterization of ribosomal RNA genes from wheat and barley.CrossRef | 1:CAS:528:DyaL3cXlsFamsQ%3D%3D&md5=8c3c6f23fca89339c281151889a2ba78CAS |

González-Elizondo MS, Peterson PM (1997) A classification of and key to the supraspecific taxa in Eleocharis (Cyperaceae). Taxon 46, 433–449.
A classification of and key to the supraspecific taxa in Eleocharis (Cyperaceae).CrossRef |

González-Elizondo MS, Tena-Flores JA (2000) Eleocharis (Cyperaceae) in the New World. In ‘Monocots: Systematics and Evolution’. (Eds KL Wilson, J Morrison) pp. 637–643. (CSIRO Publishing: Melbourne, Vic., Australia).

González Elizondo MS, Rosen DJ, Carter R, Peterson PM (2007) Eleocharis reznicekii (Cyperaceae), a new species from the Mexican High Plateau. Acta Botánica Mexicana 81, 35–43.
Eleocharis reznicekii (Cyperaceae), a new species from the Mexican High Plateau.CrossRef |

Gordon-Gray KD, Baijnath H, Ward CJ, Wragg PD (2009) Studies in Cyperaceae in southern Africa 42: pseudo-vivipary in South African Cyperaceae. South African Journal of Botany 75, 165–171.
Studies in Cyperaceae in southern Africa 42: pseudo-vivipary in South African Cyperaceae.CrossRef |

Harms LJ (1968) Cytotaxonomic studies in Eleocharis subser. Palustres: central united taxa. American Journal of Botany 55, 966–974.
Cytotaxonomic studies in Eleocharis subser. Palustres: central united taxa.CrossRef |

Hipp AL (2007) Nonuniform processes of chromosome evolution in sedges (Carex: Cyperaceae). Evolution 61, 2175–2194.
Nonuniform processes of chromosome evolution in sedges (Carex: Cyperaceae).CrossRef |

Hipp AL, Rothrockm PE, Roalson EH (2009) The evolution of chromosome arrangements in Carex (Cyperaceae). Botanical Review 75, 96–109.
The evolution of chromosome arrangements in Carex (Cyperaceae).CrossRef |

Kaur N, Datson PM, Murray BG (2011) Hybridization amongst New Zealand Schoenus (Cyperaceae)? New Zealand Journal of Botany 49, 503–507.
Hybridization amongst New Zealand Schoenus (Cyperaceae)?CrossRef |

Košnar J, Košnar J, Herbstová M, Macek P, Rejmánková E, Štech M (2010) Natural hybridization in tropical spike rushes of Eleocharis subgenus Limnochloa (Cyperaceae): evidence from morphology and DNA markers. American Journal of Botany 97, 1229–1240.
Natural hybridization in tropical spike rushes of Eleocharis subgenus Limnochloa (Cyperaceae): evidence from morphology and DNA markers.CrossRef |

Luceño M (1994) Cytotaxonomic studies in Iberian, Balearic, North African, and Macaronesian species of Carex (Cyperaceae): II. Canadian Journal of Botany 72, 587–596.
Cytotaxonomic studies in Iberian, Balearic, North African, and Macaronesian species of Carex (Cyperaceae): II.CrossRef |

Luceño M, Castroviejo S (1991) Agmatoploidy in Carex laevigata (Cyperaceae): fusion and fission of chromosomes as the mechanism of cytogenetic evolution in Iberian populations. Plant Systematics and Evolution 177, 149–159.
Agmatoploidy in Carex laevigata (Cyperaceae): fusion and fission of chromosomes as the mechanism of cytogenetic evolution in Iberian populations.CrossRef |

Luceño M, Vanzela ALL, Guerra M (1998) Cytotaxonomic studies in Brazilian Rhynchospora (Cyperaceae), a genus exhibiting holocentric chromosomes. Canadian Journal of Botany 76, 440–449.
Cytotaxonomic studies in Brazilian Rhynchospora (Cyperaceae), a genus exhibiting holocentric chromosomes.CrossRef |

Marasek A, Hasterok R, Wiejacha K, Orlikowska T (2004) Determination by GISH and FISH of hybrid status in Lilium. Hereditas 140, 1–7.
Determination by GISH and FISH of hybrid status in Lilium.CrossRef |

Marques A, Ribeiro T, Neumann P, Macas J, Novak P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, Brandt R, Vanzela ALL, Beseda T, Simková H, Pedrosa-Harand A, Houben A (2015) Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed amongst euchromatin. Proceedings of the National Academy of Sciences of the United States of America 112, 13633–13638.
Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed amongst euchromatin.CrossRef | 1:CAS:528:DC%2BC2MXhs12lurrI&md5=d913e605e698ca14e8806055a1141d40CAS |

Michelan VS, Trevisan R, da Silva CRM, Souza RF, Luceño M, Vanzela ALL (2012) Morphological and genomic characterization of Rhynchospora tenuis complex (Cyperaceae) and its taxonomic implications. Rodriguésia 63, 775–784.
Morphological and genomic characterization of Rhynchospora tenuis complex (Cyperaceae) and its taxonomic implications.CrossRef |

Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America 76, 5269–5273.
Mathematical model for studying genetic variation in terms of restriction endonucleases.CrossRef | 1:CAS:528:DyaL3cXitVWn&md5=777c35d87f1fef0657d0277f3ebd9b4bCAS |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

Rambo B (1959) Cyperaceae Riograndenses. Pesquisas 3, 354–453.

Roalson EH (2008) A synopsis of chromosome number variation in the Cyperaceae. Botanical Review 74, 209–393.
A synopsis of chromosome number variation in the Cyperaceae.CrossRef |

Roalson EH, Friar EA (2000) Infrageneric classification of Eleocharis (Cyperaceae) revisited: evidence from the internal transcribed spacer (ITS) region of nuclear ribosomal DNA. Systematic Botany 25, 323–336.
Infrageneric classification of Eleocharis (Cyperaceae) revisited: evidence from the internal transcribed spacer (ITS) region of nuclear ribosomal DNA.CrossRef |

Roalson EH, Hinchliff CE, Trevisan R, da Silva CRM (2010) Phylogenetic relationships in Eleocharis (Cyperaceae): C4 photosynthesis origins and patterns of diversification in the spikerushes. Systematic Botany 35, 257–271.
Phylogenetic relationships in Eleocharis (Cyperaceae): C4 photosynthesis origins and patterns of diversification in the spikerushes.CrossRef |

San Martin JAB, Fagundes NF, Mariath JEA (2014) Ontogeny of the proliferous spikelet in Eleocharis viridans (Cyperaceae). Botanical Journal of the Linnean Society 176, 524–539.
Ontogeny of the proliferous spikelet in Eleocharis viridans (Cyperaceae).CrossRef |

Saunte L (1958) Chromosome variation in the Heteocharis patustris–uniglumis complex. Nature 181, 1019–1020.
Chromosome variation in the Heteocharis patustris–uniglumis complex.CrossRef | 1:STN:280:DyaG1c%2FosVaquw%3D%3D&md5=db554425acfc10e68335ffbf946ff71cCAS |

Smith SG, Bruhl JJ, González-Elizondo MS, Menapace FJ (2002) Eleocharis R.Br. In ‘Flora of North America, vol. 23. Magnoliophyta: Commelinidae (in part) Cyperaceae’. (Ed. Flora of North America Editorial Committee) pp. 60–120. (Oxford University Press: New York, NY, USA)

Sousa A, Barros e Silva AE, Cuadrado A, Loarce Y, Alves MV, Guerra M (2011) Distribution of 5S and 45S rDNA sites in plants with holokinetic chromosomes and the ‘chromosome field’ hypothesis. Micron (Oxford, England) 42, 625–631.
Distribution of 5S and 45S rDNA sites in plants with holokinetic chromosomes and the ‘chromosome field’ hypothesis.CrossRef | 1:CAS:528:DC%2BC3MXlvFCqsbw%3D&md5=c92d09b0b1bc5e79c52f190bd9228705CAS |

Strandhede SO (1965) Chromosome studies in Eleocharis, subser. Palustres. III. Observations on western European taxa. Opera Botanica 9, 1–86.

Strandhede SO (1966) Morphologic variation and taxonomy in European Eleocharis, subser. Palustres. Opera Botanica 10, 1–187.

Svenson HK (1939) Monographic studies in the senus Eleocharis V. Rhodora 41, 1–110.

Trevisan R, Boldrini II (2008) O gênero Eleocharis R.Br. (Cyperaceae) no Rio Grande do Sul, Brasil. Revista Brasileira de Biociências 6, 7–67.

Trevisan R, Boldrini II (2010) Novelties in Eleocharis ser. Tenuissimae (Cyperaceae), and a key to the species of the series occurring in Brazil. Systematic Botany 35, 504–511.
Novelties in Eleocharis ser. Tenuissimae (Cyperaceae), and a key to the species of the series occurring in Brazil.CrossRef |

Van de Peer Y, Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Computer Applications in the Biosciences 10, 569–570.

Vanzela ALL, Colaço W (2002) Mitotic and meiotic behavior of γ irradiated holocentric. chromosomes of Rhynchospora pubera (Cyperaceae). Acta Scientiarum 24, 611–614.

Vanzela ALL, Cuadrado A, Jouve N, Luceño M, Guerra M (1998) Multiple locations of the rDNA sites in holocentric chromosomes of Rhynchospora (Cyperaceae). Chromosome Research 6, 345–350.
Multiple locations of the rDNA sites in holocentric chromosomes of Rhynchospora (Cyperaceae).CrossRef | 1:CAS:528:DyaK1MXhsF2q&md5=089be1eaa49eb61c1413b622d4795d9cCAS |

Vanzela ALL, Cuadrado A, Guerra M (2003) Localization of 45S rDNA and telomeric sites on holocentric chromosomes of Rhynchospora tenuis Link (Cyperaceae). Genetics and Molecular Biology 26, 199–201.
Localization of 45S rDNA and telomeric sites on holocentric chromosomes of Rhynchospora tenuis Link (Cyperaceae).CrossRef | 1:CAS:528:DC%2BD3sXmsV2lsLk%3D&md5=c31dcc2021fe32432f0543a2424e2e8eCAS |

Więcław H, Wilhelm M (2014) Natural hybridization within the Carex flava complex (Cyperaceae) in Poland: morphometric studies. Annales Botanici Fennici 51, 129–147.
Natural hybridization within the Carex flava complex (Cyperaceae) in Poland: morphometric studies.CrossRef |

Yang M, Zhou Y, Zhu Q, Zhang W (2009) AFLP markers in the detection of Scirpus × mariqueter (CYPERACEAE) hybrid in China. Aquatic Botany 91, 298–302.
AFLP markers in the detection of Scirpus × mariqueter (CYPERACEAE) hybrid in China.CrossRef | 1:CAS:528:DC%2BD1MXhtFKntr3M&md5=420c87553a1f9fa2d2535a250ea23c7eCAS |



Supplementary MaterialSupplementary Material (337 KB) Export Citation