Evolution of Genome Size and Chromosome Number in The

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Evolution of Genome Size and Chromosome Number in The Annals of Botany 114: 1651–1663, 2014 doi:10.1093/aob/mcu189, available online at www.aob.oxfordjournals.org 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 Fleischmann1,*, Todd P. Michael2, Fernando Rivadavia3, Aretuza Sousa1, Wenqin Wang2, Eva M. Temsch4, Johann Greilhuber4, Kai F. Mu¨ller5 and Gu¨nther Heubl1 1Department of Biology, Systematic Botany and Mycology and Geo-Bio Center LMU, Ludwig-Maximilians-Universita¨t Downloaded from Mu¨nchen, Menzinger Strasse 67, D 80638 Munich, Germany, 2Waksman Institute of Microbiology, Rutgers University, 190 Frelinghuysen Road, Piscataway, NJ 08854, USA, 31 Daniel Burnham Ct, San Francisco, CA 94109, USA, 4Department of Botany and Biodiversity Research, Faculty of Life Sciences, University of Vienna, Rennweg 14, A 1030 Vienna, Austria and 5Institute for Evolution and Biodiversity, University of Muenster, Hu¨fferstrasse 1, D 48149 Mu¨nster, Germany * For correspondence. E-mail fl[email protected] http://aob.oxfordjournals.org/ Received: 3 July 2014 Returned for revision: 9 July 2014 Accepted: 7 August 2014 Published electronically: 1 October 2014 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 chromo- some 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 sizewith chromosome number and size, with the phylogenyof the group and with growth at University of Wisconsin-Madison Libraries on February 16, 2015 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 measure- ments 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 (2¼n 36, 38) are documented for three derived taxa. The¼ different¼ ploidy levels¼ corresponded¼ to the two subgenera, but¼ were not directly correlated to differ- ences 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). ≈ ConclusionsGenlisea is an idealcandidatemodel≈ organism for the understandingof genome reductionasthe genus †includes species with both relatively large ( 1700 Mbp) and ultrasmall ( 61 Mbp) genomes. This comparative, phylogeny-basedanalysis of genome sizes andkaryotypesin" Genlisea providesessential" datafor 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. Key words: Bladderwort, carnivorous plant, chromosome number, flow cytometry, Genlisea, genome miniaturization, genome size, Lentibulariaceae, Lamiales. INTRODUCTION swollen vesicle (‘stomach’) followed by a long tubular ‘neck’, which is dichotomously forked at the apex into two helically The carnivorous corkscrew plants, Genlisea (Order Lamiales, twisted, hollow arms (Fig. 1A). Lentibulariaceae, bladderwort family) comprise 29 species Since its discovery .200 years ago, Genlisea has remained (Fleischmann, 2012), which are distributed from South to the most understudied and poorly known genus among otherwise Central America and in Africa. The plants are annual or perennial well-studied carnivorous plant genera. This is mainly due to its herbs, strictly heterophyllous, producing spathulate, green, distribution across remote areas and the difficulty of accessing photosynthetic epiterrestrial leaves and achlorophyllous subter- living plant material. Although the carnivorous nature of ranean tubular leaves (rhizophylls). The latter constitute the car- Genlisea was postulated as early as 1875 by Charles Darwin nivorous traps of the plant, and consist of a basal stalk and a (Darwin, 1875), with an alleged specialization for trapping # The Author 2014. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 1652 Fleischmann et al. — Genome sizes and chromosome numbers in Genlisea into an 24-fold variation in genome size (Greilhuber et al., A B 2006). Genome" sizes have been recorded for several species of the sister genus Utricularia and the common sister Pinguicula, all falling within a range (of 1099 Mbp) that lies between the ultrasmall and the larger genomes" of Genlisea (Greilhuber et al., 2006; Veleba et al., 2014). Within the genus Genlisea, genome sizes range from 63.4 to 1510 Mbp (Greilhuber et al., 2006; Veleba et al., 2014), and in different populations investi- gated for a few taxa (most notably G. aurea) genome size can vary up to 2-fold (Albert et al., 2010). Very few cytological studies have been carried out for Lentibulariaceae thus far, and these have predominantly Downloaded from focused on Pinguicula (summarized by Casper and Stimper, 2009) oraquatic species of Utricularia section Utricularia (sum- C D marized by Casper and Manitz, 1975 and Rahman et al., 2001). In the case of Genlisea, chromosome numbers have been reported for only five species so far (Greilhuber et al., 2006; Vu et al., 2012), but three of these represent approximations http://aob.oxfordjournals.org/ only. The general lack of karyotype data available for Utricularia and Genlisea is mainly due to the very small size of their metaphase chromosomes (Reese, 1951; Kondo, 1972a; Rahman et al., 2001; Greilhuberet al., 2006), because of difficul- ties in staining these chromosomes with standard dyes (Rahman et al., 2001; A. Fleischmann, A. Sousa and J. Greilhuber, pers. obs.), but also because of the difficulty of obtaining suitable living material of most taxa for chromosome counts. The F IG. 1. (A) Growth habit of Genlisea (an excavated plant of G. flexuosa is shown) at University of Wisconsin-Madison Libraries on February 16, 2015 illustratingthe green photosyntheticleaves andthe palewhite, subterranean carniv- present study was only possible because a large sampling of cul- orous trap leaves ( rhizophylls). (B) Inflorescence of Genlisea (G. aurea var. tivated species of Genlisea was available to the authors. All minor is shown). The¼ most apical, juvenile flower buds (*, with the sepals still species of Genlisea and Utricularia lack roots entirely, and there- touching each other at their tips) bear anthers at the right stage of development, fore shoot apices have to be used to perform somatic chromosome with pollen mother cells suitable for meiotic chromosome counts. (C, D) Two stages of young, developing rhizophylls used for mitotic chromosome counts. counts in these two genera (Tanaka and Uchiyama, 1988; Rahman Only the apical tips of the rhizophylls (arrows) containing meristematic cells et al., 2001) when flowering material is not available for meiotic/ (visible as milky white tissue) were used for preparation. Scale bars 1cm. mitotic chromosome counts (however, flower buds were used ¼ to obtain the majority of karyotypes published so far, by protozoa and various other small soil organisms (Goebel, 1891; Subramanyam and Kamble, 1968; Kondo, 1972a, b; Casper and Barthlott et al., 1998; Płachno et al., 2008; Darnowski and Fritz, Manitz, 1975; Greilhuber et al., 2006). In the present work, rhizo- 2010; Fleischmann, 2012), the underlying mechanism of trap phyll shootapices were used forcytological studies inGenliseafor functioning remains unclear (Adamec, 2003; Fleischmann, the first time. 2012). A major focus of the present work wasto study the evolution of One of the biggest surprises, which brought the rather elu- genome sizes and chromosome numbers in a phylogenetic con- sive genusto the interest of the scientific community, was the dis- text. The genome sizes, given as 1C values, were measured from covery that some species of Genlisea possess ultrasmall nuclear cultivated plant material for 20 accessions (representing 12 taxa genomes (holoploid genome size 60–64 Mbp in some strains of the genus, or 40 % of the total species number), with represen- of G. aurea; Greilhuber et al., 2006"; Albert et al., 2010; Leushkin tatives from both subgenera and all four sections (Fleischmann et al., 2013), the smallest known among angiosperms (Greilhuber et al., 2010; Fleischmann, 2012), using flow cytometry. et al., 2006; Bennett
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