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

Genetic variation in Trithuria inconspicua and T. filamentosa (Hydatellaceae): a new subspecies and a hypothesis of apomixis arising within a predominantly selfing lineage

Rob D. Smissen https://orcid.org/0000-0001-6299-1987 A C , Kerry A. Ford A , Paul D. Champion B and Peter B. Heenan A
+ Author Affiliations
- Author Affiliations

A Allan Herbarium, Landcare Research, PO Box 69040, Lincoln, 7608, New Zealand.

B National Institute of Water and Atmospheric Research (NIWA), PO Box 11-115, Hamilton, 3251, New Zealand.

C Corresponding author. Email: smissenr@landcareresearch.co.nz

Australian Systematic Botany 32(1) 1-11 https://doi.org/10.1071/SB18013
Submitted: 19 March 2018  Accepted: 24 November 2018   Published: 31 January 2019

Abstract

While examining herbarium specimens of Trithuria inconspicua Cheeseman, we observed differences in the stigmatic hairs among plants from New Zealand’s North and South Islands. This motivated us to assess genetic and morphological variation within this species and its sister T. filamentosa Rodway from Tasmania. Samples were collected from lakes in the three disjunct geographic areas where the two species occur. Genetic variation in both species was assessed with simple sequence-repeat (SSR, microsatellite) markers and analyses of genetic distances. We also compared the morphology of northern and southern New Zealand T. inconspicua using fresh material. Samples of each species clustered together in a minimum evolution tree built from genetic distances. Trithuria filamentosa had more genetic diversity than did T. inconspicua. Within T. inconspicua, plants from lakes in the North Island and the South Island formed discrete genetic groups diagnosable by subtle morphological differences. Low levels of heterozygosity in both species are consistent with a high level of selfing, as suggested for other co-sexual Trithuria species, but unusual for a putative apomict. On the basis of genetic and morphological variation, we propose recognition of the northern New Zealand and southern New Zealand lineages of T. inconspicua at subspecies rank.


References

Bicknell RA, Koltunow AM (2004) Understanding apomixis: recent advances and remaining conundrums. The Plant Cell 16, S228–S245.
Understanding apomixis: recent advances and remaining conundrums.Crossref | GoogleScholarGoogle Scholar | 15131250PubMed |

Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31, 25–28.
M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods.Crossref | GoogleScholarGoogle Scholar |

de Lange PJ, Murray BG, Datson PM (2004) Contributions to a chromosome atlas of the New Zealand flora: 38. Counts for 50 families. New Zealand Journal of Botany 42, 873–904.
Contributions to a chromosome atlas of the New Zealand flora: 38. Counts for 50 families.Crossref | GoogleScholarGoogle Scholar |

de Lange PJ, Rolfe JR, Champion PD, Courtney SP, Heenan PB, Barkla JW, Cameron EK, Norton DA, Hitchmough RA (2013) ‘Conservation Status of New Zealand Indigenous Vascular Plants, (2012 revision). New Zealand Threat Classification Series 3.’ (Department of Conservation: Wellington, New Zealand)

de Lange PJ, Rolfe JR, Barkla JW, Courtney SP, Champion PD, Perrie LR, Beadel SM, Ford KA, Breitwieser I, Schönberger I, Hindmarsh-Walls R, Heenan PB, Ladley K (2018) ‘Conservation Status of New Zealand Indigenous Vascular Plants, 2017. New Zealand Threat Classification Series 22.’ (Department of Conservation: Wellington, New Zealand)

Doyle JJ, Dickson EE (1987) Preservation of plant samples for DNA restriction endonuclease analysis. Taxon 36, 715–722.
Preservation of plant samples for DNA restriction endonuclease analysis.Crossref | GoogleScholarGoogle Scholar |

Duretto MF (Ed.) (2011) 1 Hydatellaceae, 2011:1. In ‘Flora of Tasmania Online’. (Tasmanian Herbarium, Tasmanian Museum and Art Gallery: Hobart, Tas., Australia) Available at http://demo1.tmag.tas.gov.au/treatments/families/Hydatellaceae/Hydatellaceae_2011_1.pdf [Verified 19 October 2018]

Edgar E (1966) The male flowers of Hydatella inconspicua (Cheesem.) Cheesem. (Centrolepidaceae). New Zealand Journal of Botany 4, 153–158.
The male flowers of Hydatella inconspicua (Cheesem.) Cheesem. (Centrolepidaceae).Crossref | GoogleScholarGoogle Scholar |

Edgar E (1970) Centrolepidaceae. In ‘Flora of New Zealand. Vol. 2. Indigenous Tracheophyta: Monocotyledons except Gramineae’. (Eds LB Moore, E Edgar) pp. 79–85. (Government Printer: Wellington, New Zealand)

Faircloth BC (2008) MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Molecular Ecology Resources 8, 92–94.
MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design.Crossref | GoogleScholarGoogle Scholar | 21585724PubMed |

Friedman EF, Bachelier JB, Hormaza JI (2012) Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early diverging flowering plants. American Journal of Botany 99, 1083–1095.
Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early diverging flowering plants.Crossref | GoogleScholarGoogle Scholar |

Godley EJ (1998) Biographical notes (29): Harry Carse (1857–1930). New Zealand Botanical Society Newsletter 51, 13–19.

Hamann U (1976) Hydatellaceae: a new family of Monocotyledoneae. New Zealand Journal of Botany 14, 193–196.
Hydatellaceae: a new family of Monocotyledoneae.Crossref | GoogleScholarGoogle Scholar |

Hörandl E (2010) The evolution of self-fertility in apomictic plants. Sexual Plant Reproduction 23, 73–86.
The evolution of self-fertility in apomictic plants.Crossref | GoogleScholarGoogle Scholar | 20165965PubMed |

Iles WJD, Rudall PJ, Sokoloff DD, Remizowa MV, MacFarlane TD, Logacheva MD, Graham SW (2012) Molecular phylogenetics of Hydatellaceae (Nymphaeales): sexual-system homoplasy and a new sectional classification. American Journal of Botany 99, 663–676.
Molecular phylogenetics of Hydatellaceae (Nymphaeales): sexual-system homoplasy and a new sectional classification.Crossref | GoogleScholarGoogle Scholar |

Iles WJD, Lee C, Sokoloff DD, Remizowa MV, Yadav SR, Barrett MD, Barrett RL, MacFarlane TD, Logacheva MD, Rudall PJ, Graham SW (2014) Reconstructing the age of the ancient flowering-plant family Hydatellaceae (Nymphaeales). BMC Evolutionary Biology 14, 102
Reconstructing the age of the ancient flowering-plant family Hydatellaceae (Nymphaeales).Crossref | GoogleScholarGoogle Scholar |

Kynast RG, Joseph JA, Pellicer J, Ramsay MM (2014) Chromosome behaviour at the base of the angiosperm radiation: karyology of Trithuria submersa (Hydatellacaeae, Nymphaeales). Annals of Botany 101, 1447–1455.
Chromosome behaviour at the base of the angiosperm radiation: karyology of Trithuria submersa (Hydatellacaeae, Nymphaeales).Crossref | GoogleScholarGoogle Scholar |

Le Comber SC, Ainouche ML, Kovarik A, Leitch AR (2010) Making a functional diploid: from polysomic to disomic inheritance. New Phytologist 186, 113–122.
Making a functional diploid: from polysomic to disomic inheritance.Crossref | GoogleScholarGoogle Scholar | 20028473PubMed |

Marques I, Montgomery SA, Barker MS, MacFarlane TD, Conran JG, Catalan P, Rieseberg LH, Rudall PJ, Graham SW (2016) Transcriptome-derived evidence supports recent polypoloidization and a major phylogeographic division in Trithuria submersa (Hydatellaceae, Nymphaeales). New Phytologist 210, 310–323.
Transcriptome-derived evidence supports recent polypoloidization and a major phylogeographic division in Trithuria submersa (Hydatellaceae, Nymphaeales).Crossref | GoogleScholarGoogle Scholar | 26612464PubMed |

Morgan-Richards M, Trewick SA, Chapman HM, Krachulcova A (2004) Interspecific hybridization among Hieracium species in New Zealand: evidence from flow cytometry. Heredity 93, 34–42.
Interspecific hybridization among Hieracium species in New Zealand: evidence from flow cytometry.Crossref | GoogleScholarGoogle Scholar | 15138450PubMed |

Pfeiffer T, Roschanski AM, Pannell JR, Korbecka G, Schnittler M (2011) Characterization of microsatellite loci and reliable genotyping in a polyploid plant, Mercuralis perennis (Euphorbiaceae). The Journal of Heredity 102, 479–488.
Characterization of microsatellite loci and reliable genotyping in a polyploid plant, Mercuralis perennis (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar | 21576288PubMed |

Pledge DH (1974) Some observations on Hydatella inconspicua (Cheesem.) Cheesem. (Centrolepidaceae). New Zealand Journal of Botany 12, 559–561.
Some observations on Hydatella inconspicua (Cheesem.) Cheesem. (Centrolepidaceae).Crossref | GoogleScholarGoogle Scholar |

Prychid CJ, Sokoloff DD, Remizowa MV, Tuckett RW, Yadav SR, Rudall PJ (2011) Unique stigmatic hairs and pollen-tube growth within the stigmatic cell wall in the early divergent angiosperm family Hydatellaceae. Annals of Botany 108, 599–608.
Unique stigmatic hairs and pollen-tube growth within the stigmatic cell wall in the early divergent angiosperm family Hydatellaceae.Crossref | GoogleScholarGoogle Scholar | 21320877PubMed |

Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics Methods and Protocols: Methods in Molecular Biology, Vol. 132’. (Eds S Krawetz, S Misener) pp. 365–386 (Humana Press: Totowa, NJ, USA)

Rudall PJ, Sokoloff DD, Remizowa MV, Conran JG, Davis JI, Macfarlane TD, Stevenson DW (2007) Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early divergent angiosperm lineage. American Journal of Botany 94, 1073–1092.
Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early divergent angiosperm lineage.Crossref | GoogleScholarGoogle Scholar | 21636477PubMed |

Rudall PJ, Remizowa MV, Beer AS, Bradshaw E, Stevenson DW, Macfarlane TD, Tuckett RE, Yadav SR, Sokoloff DD (2008) Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. American Journal of Botany 101, 941–956.

Rudall PJ, Eldridge T, Tratt J, Ramsay MM, Tuckett RE, Smith SY, Collinson ME, Remizowa MV, Sokoloff DD (2009) Seed fertilization, development, and germination in Hydatellacae (Nymphaeales): implications for endosperm evolution in early angiosperms. American Journal of Botany 96, 1581–1593.
Seed fertilization, development, and germination in Hydatellacae (Nymphaeales): implications for endosperm evolution in early angiosperms.Crossref | GoogleScholarGoogle Scholar | 21622344PubMed |

Saarela JM, Rai HS, Doyle JA, Endress PK, Mathews S, Marchant AD, Briggs BG, Graham SW (2007) Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446, 312–315.
Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree.Crossref | GoogleScholarGoogle Scholar | 17361182PubMed |

Sokoloff DD, Remizowa MV, Macfarlane TD, Rudall PJ (2008a) Classification of the early divergent angiosperm family Hydatellaceae: one genus instead of two, four new species and sexual dimorphism in dioecious taxa. Taxon 57, 179–200.

Sokoloff DD, Remizowa MV, Macfarlane TD, Tuckett RE, Ramsay MM, Beer AS, Yadav SR, Rudall PJ (2008b) Seedling diversity in Hydatellaceae: implications for the evolution of angiosperm cotyledons. Annals of Botany 101, 153–164.
Seedling diversity in Hydatellaceae: implications for the evolution of angiosperm cotyledons.Crossref | GoogleScholarGoogle Scholar | 18032428PubMed |

Sokoloff DD, Remizowa MV, Briggs BG, Rudall PJ (2009) Shoot architecture and branching pattern in perennial Hydatellaceae (Nymphaeales). International Journal of Plant Sciences 170, 869–884.
Shoot architecture and branching pattern in perennial Hydatellaceae (Nymphaeales).Crossref | GoogleScholarGoogle Scholar |

Sokoloff DD, Remizowa MV, Macfarlane TD, Conran JG, Yadav SR, Rudall PJ (2013) Comparative fruit sturcture in Hydatellaceae (Nymphaeales) reveals specialized pericarp dehiscence in some early divergent angiosperms with ascidiate carpels. Taxon 62, 40–61.

Sokoloff DD, Remizowa MV, Conran JG, Macfarlane TD, Ramsay MM, Rudall PJ (2014) Embryo and seedling morphology in Trithuria lanterna (Hydatellaceae, Nymphaeales): new data for infrafamilial systematics and a novel type of syncotyly. Botanical Journal of the Linnean Society 174, 551–573.
Embryo and seedling morphology in Trithuria lanterna (Hydatellaceae, Nymphaeales): new data for infrafamilial systematics and a novel type of syncotyly.Crossref | GoogleScholarGoogle Scholar |

Swofford DL (2003) ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.’ (Sinauer Associates: Sunderland, MA, USA)

Tasmanian Government, Department of Primary Industries, Parks, Water and Environment (2014) Threatened species: vascular plants. Available at https://dpipwe.tas.gov.au/conservation/threatened-species-and-communities/lists-of-threatened-species/threatened-species-vascular-plants [Verified 19 October 2018].

Taylor ML (2011) Developmental evolution of the progamic phase in Nymphaeales. PhD thesis, University of Tennessee, Knoxville, TN, USA.

Taylor ML, Williams JH (2012) Pollen tube development in two species of Trithuria (Hydatellaceae) with contrasting breeding systems. Sexual Plant Reproduction 25, 83–96.
Pollen tube development in two species of Trithuria (Hydatellaceae) with contrasting breeding systems.Crossref | GoogleScholarGoogle Scholar | 22367232PubMed |

Taylor ML, Macfarlane TD, Williams JH (2010) Reproductive ecology of the basal angiosperm Trithuria submersa (Hydatellaceae). Annals of Botany 106, 909–920.
Reproductive ecology of the basal angiosperm Trithuria submersa (Hydatellaceae).Crossref | GoogleScholarGoogle Scholar | 21047886PubMed |

Townsend AJ, de Lange PJ, Duffy CAJ, Miskelly CM, Molloy J, Norton DA (2008) ‘New Zealand Threat Classification Manual.’ (Science & Technical Publishing, Department of Conservation: Wellington, New Zealand)

Wells RDS, Clayton JS, de Winton MD (1998) Submerged vegetation of Lakes Te Anau, Manapōuri, Monowai, Hauroko, and Poteriteri, Fiordland, New Zealand. New Zealand Journal of Marine and Freshwater Research 32, 621–638.
Submerged vegetation of Lakes Te Anau, Manapōuri, Monowai, Hauroko, and Poteriteri, Fiordland, New Zealand.Crossref | GoogleScholarGoogle Scholar |