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, 114 (8), 1651-63

Evolution of Genome Size and Chromosome Number in the Carnivorous Plant Genus Genlisea (Lentibulariaceae), With a New Estimate of the Minimum Genome Size in Angiosperms

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Evolution of Genome Size and Chromosome Number in the Carnivorous Plant Genus Genlisea (Lentibulariaceae), With a New Estimate of the Minimum Genome Size in Angiosperms

Andreas Fleischmann et al. Ann Bot.

Abstract

Background and aims: Some species of Genlisea possess ultrasmall nuclear genomes, the smallest known among angiosperms, and some have been found to have chromosomes of diminutive size, which may explain why chromosome numbers and karyotypes are not known for the majority of species of the genus. However, other members of the genus do not possess ultrasmall genomes, nor do most taxa studied in related genera of the family or order. This study therefore examined the evolution of genome sizes and chromosome numbers in Genlisea in a phylogenetic context. The correlations of genome size with chromosome number and size, with the phylogeny of the group and with growth forms and habitats were also examined.

Methods: Nuclear genome sizes were measured from cultivated plant material for a comprehensive sampling of taxa, including nearly half of all species of Genlisea and representing all major lineages. Flow cytometric measurements were conducted in parallel in two laboratories in order to compare the consistency of different methods and controls. Chromosome counts were performed for the majority of taxa, comparing different staining techniques for the ultrasmall chromosomes.

Key results: Genome sizes of 15 taxa of Genlisea are presented and interpreted in a phylogenetic context. A high degree of congruence was found between genome size distribution and the major phylogenetic lineages. Ultrasmall genomes with 1C values of <100 Mbp were almost exclusively found in a derived lineage of South American species. The ancestral haploid chromosome number was inferred to be n = 8. Chromosome numbers in Genlisea ranged from 2n = 2x = 16 to 2n = 4x = 32. Ascendant dysploid series (2n = 36, 38) are documented for three derived taxa. The different ploidy levels corresponded to the two subgenera, but were not directly correlated to differences in genome size; the three different karyotype ranges mirrored the different sections of the genus. The smallest known plant genomes were not found in G. margaretae, as previously reported, but in G. tuberosa (1C ≈ 61 Mbp) and some strains of G. aurea (1C ≈ 64 Mbp).

Conclusions: Genlisea is an ideal candidate model organism for the understanding of genome reduction as the genus includes species with both relatively large (∼1700 Mbp) and ultrasmall (∼61 Mbp) genomes. This comparative, phylogeny-based analysis of genome sizes and karyotypes in Genlisea provides essential data for selection of suitable species for comparative whole-genome analyses, as well as for further studies on both the molecular and cytogenetic basis of genome reduction in plants.

Keywords: Bladderwort; Genlisea; Lamiales; Lentibulariaceae; carnivorous plant; chromosome number; flow cytometry; genome miniaturization; genome size.

Figures

Fig. 1.
Fig. 1.
(A) Growth habit of Genlisea (an excavated plant of G. flexuosa is shown) illustrating the green photosynthetic leaves and the pale white, subterranean carnivorous trap leaves (=rhizophylls). (B) Inflorescence of Genlisea (G. aurea var. minor is shown). The most apical, juvenile flower buds (*, with the sepals still touching each other at their tips) bear anthers at the right stage of development, with pollen mother cells suitable for meiotic chromosome counts. (C, D) Two stages of young, developing rhizophylls used for mitotic chromosome counts. Only the apical tips of the rhizophylls (arrows) containing meristematic cells (visible as milky white tissue) were used for preparation. Scale bars = 1 cm.
Fig. 2.
Fig. 2.
Light microscope photographs and camera lucida drawings of orcein-stained mitotic prophase plates from rhizophyll tip meristems of Genlisea spp. (A, B) G. uncinata, 2n = 16. (C, D) G. metallica, 2n = 16. (E, F) G. violacea from Couto de Magalhães, 2n = 16. (G, H) G. flexuosa, 2n = 16. (J, K) G. hispidula, 2n = 32. (L, M) G. subglabra, 2n = 32. (N, O) G. guianensis, 2n ∼40. Scale bars = 3 μm.
Fig. 3.
Fig. 3.
Metaphase chromosomes from pollen mother cells of Genlisea spp., stained with DAPI. (A–C) G. margaretae from Zambia, n = 18, 19. (C) Two meiotic metaphase cells. (D–F) G. aurea var. minor from Itacambira, pre-meiotic mitosis cells, 2n = 46. Note the smaller chromosome size compared with G. margaretae. (F) DAPI-stained interphase nuclei. Nucleoli (*) can be identified as DAPI-negative regions surrounded by more DAPI-positive DNA staining. Scale bars = 10 μm.
Fig. 4.
Fig. 4.
Genome size variation and karyotype evolution in Genlisea. DNA 1C values of studied species and a phylogenetic tree based on molecular sequence data of three chloroplast loci (Fleischmann et al., 2010); the phylogenetic position of G. tuberosa is based on unpublished rps16 and trnQ-rps16 sequence data (deposited at GenBank, accession numbers KF952604 and KF952605); only tree branches that had maximal statistic support (bootstrap value >90, Bayesian posterior probability = 1) are shown as resolved; chromosome base numbers and suggested ploidy levels are shown on the respective branches of monophyletic groups. The range of 1C DNA content and chromosome numbers for the Lentibulariaceae outgroup taxa Pinguicula and Utricularia are taken from Greilhuber et al. (2006) and from Casper and Manitz (1975), Rahman et al. (2001) and Casper and Stimper (2009), respectively, 1C values for Genlisea uncinata are from Greilhuber et al. (2006) and those for G. nigrocaulis are from Vu et al. (2012).
Fig. 5.
Fig. 5.
Evolutionary decrease in genome size in Genlisea. The species are arranged in phylogenetic order on the x-axis, from basal branching (left) to derived taxa (right; following Fleischmann et al. 2010); their average 1C values are shown on the y-axis. The 1C values obtained as size estimates from flow cytometry measurements at Rutgers are marked ‘(R)’. The respective 2n number is indicated where known. Genome sizes of taxa marked with an asterisk are taken from the literature (Greilhuber et al., 2006; Vu et al., 2012). For abbreviations of location data, see vouchers in Table 1.

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