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Variation in Genome Size in the Valeriana Officinalis Complex Resulting from Multiple Chromosomal Evolutionary Processes

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Variation in Genome Size in the Valeriana Officinalis Complex Resulting from Multiple Chromosomal Evolutionary Processes Preslia 89: 41–61, 2017 41 Variation in genome size in the Valeriana officinalis complex resulting from multiple chromosomal evolutionary processes Variabilita ve velikosti genomu Valeriana officinalis jako výsledek mnohočetných evolučních procesů Sabine B r e s s l e r1,ValerieKlatte-Asselmeyer1, Alice F i s c h e r1, Juraj P a u l e2 & Christoph D o b e š1,3* 1Department of Pharmacognosy, Pharmacobotany, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria, e-mail: [email protected], [email protected]; [email protected]; 2Department of Botany and Molecular Evolution, Senckenberg Research Institute & Natural History Museum, Senckenberganlage 25, D-60325 Frank- furt/Main, Germany, e-mail: [email protected]; 3Austrian Research Centre for Forests, Department of Forest Genetics, Seckendorff-Gudent-Weg 8, A-1131 Vienna, Austria, e-mail: [email protected]; *corresponding author Bressler S., Klatte-Asselmeyer V., Fischer A., Paule J. & Dobeš C. (2017): Variation in genome size in the Valeriana officinalis complex resulting from multiple chromosomal evolutionary pro- cesses. – Preslia 89: 41–61. Polyploidy, aneuploidy and change in DNA content of monoploid genomes or chromosomes are the principal causes of the variation in genome size. We studied these phenomena in central-European populations of the Valeriana officinalis complex in order to identify mechanisms or forces driving its evolution. The complex comprises di-, tetra- and octoploid morphologically defined so-called taxonomic “types”. Within the study area there are also intermediate “transitional types” the exis- tence of which hampers the application of traditional taxonomic concepts. We thus chose AFLP genotyping and admixture analyses to identify the genetic structuring of the material studied. Di- (2x), tetra-(4x) and octoploidy (8x) were confirmed as major ploidy levels. Major genetic clusters roughly corresponded to these ploidy levels (for K = 2: 2x- and 8x-clusters, for K = 4 with nearly identical probability: 2x-, 4x-, 8x- and unspecific clusters were identified), which further more sig- nificantly differed from each other in monoploid absolute genome size (mean 1Cx for 2x = 1.48 pg, 4x 1.29 pg, 8x 1.10 pg). Several individuals of all ploidy levels were admixed, particularly tetraploids. Relative genome size (the sample: standard DAPI fluorescence) was positively corre- lated with the proportion of the diploid genetic cluster shared by the tetraploids, indicating that hybridization caused the variation in genome size. This result is in accordance with the significant negative correlation of the genome size of tetraploids with their geographic distance to the diploids. However, remarkable intra-ploidy variation in relative genome size was recorded for all ploidy levels (1.14-fold in diploids, 1.28-fold in tetraploids, 1.19-fold in octoploids). We identified aneuploidy as an additional source of variation in genome size in the di- and tetraploids. The contri- bution of extra chromosomes to absolute genome size exceeded the observed variation within euploids in the diploids, whereas it was included in the regular variability in genome size recorded for the eutetraploids. Variation in monoploid genome size was recorded in polyploids but not in di- ploids, indicating that polyploids experienced higher dynamics in the evolution of their genomes. Finally, 38.0–63.2% of the total intra-ploidy variation in relative genome size occurred within populations. In conclusion, the Valeriana officinalis complex provides an example of variation in genome size due to four principal evolutionary forces: polyploidization, change in chromosome number and in DNA content of chromosomes and (secondarily) hybridization, but their relative importance differed among ploidy levels. Although the stability in the size of the monoploid genome in species is considered to be the standard case, we found great variability within popula- tions suggesting that genome size is variable even within narrowly defined taxa. doi: 10.23855/preslia.2017.041 42 Preslia 89: 41–61, 2017 K e y w o r d s: aneuploidy, AFLP, chromosome number, evolution, flow cytometry, genome size, hybridization, polyploidy, population, Valeriana Introduction Data on genome size are available for an increasing number of plant species and deemed of great evolutionary importance and taxonomic significance. Variation in genome size is associated with ecological preferences (Reeves et al. 1998, Jakob et al. 2004) or toler- ances (Macgillivray & Grime 1995), generation time (Bennett 1972), cell size (Kondorosi et al. 2000), rates of speciation (Jakob et al. 2004, Soltis et al. 2009) and spe- cies limits (Ohri 1998, Soltis et al. 2007). Currently genome size is known for about 8500 species of plants (http://data.kew.org/cvalues) and varies by a factor of nearly 2400 in angiosperms (Bennett & Leitch 1995, 2011). Variation in genome size is generated by three principal mechanisms: polyploidi- zation, deletion or proliferation of DNA and gain or loss of single chromosomes (i.e. aneuploidy). Polyploidy refers to the presence of more than two basic chromosome sets (i.e. monoploid genomes: Greilhuber 2005b) within a single cell nucleus, either due to genome multiplication within a species (i.e. autopolyploidization) or in association with interspecific hybridization (i.e. allopolyploidization: Ramsey & Schemske 1998). Genome size in polyploids may add up to the sum of the DNA amounts of the inherited monoploid progenitor genomes (Levin 2002, Leitch & Bennett 2004). However, polyploidization has been shown to trigger changes in the size (and structure) of plant genomes frequently leading to a decrease in DNA content per monoploid genome in polyploids compared to the diploid progenitors (Leitch & Bennett 2004). Molecular mechanisms generating genome downsizing comprise transposon activation, excessive homologous pairing of chromosomes, or specific elimination of genes and DNA sequences (Soltis & Soltis 1999, Leitch & Bennett 2004, Soltis et al. 2009). Aneuploidy, a chromosome number that differs from a multiple of the base chromosome number due to non-balanced gain or loss of whole chromosomes, finally, arises as a result of chromo- some missegregation (e.g. Compton 2011). Aneuploidy is also associated with the occur- rence of B chromosomes (Guerra 2008), which originate and are maintained through specific evolutionary mechanisms (Camacho et al. 2000). A fourth evolutionary force that brings about change in genome size is hybridization among individuals that differ in their nuclear DNA content. Additivity of parental genomes provides a basis for the identification of primary hybrids and later hybrid gener- ations provided that parents are sufficiently differentiated to allow for the separation of genomes intermediate in size. Approaches applied involve reconstruction of the actual process of hybridization by comparison of genome sizes observed and expected in a given situation and evolutionary scenario (e.g. the genome size of the F1 expected from the fusion of meiotically reduced parental gametes), and correlation of genome size with data providing independent evidence for hybridization, like the morphological differenti- ation of parents (Ekrt et al. 2010, Vít et al. 2014). The use of flow cytometry (FCM) has made it much faster and convenient to deter- mine the genome size of plants (Doležel et al. 1998, Suda 2004, Shapiro 2007). However, its application requires special care to avoid methodological pitfalls (Greilhuber 2005a). GenomesizeinValeriana officinalis 43 A particular challenge for the application of FCM in plants is the effect of secondary metabolites on the measurement. Endogenous metabolites such as phenolic substances (e.g. tannins, flavonoids, anthocyans, cumarins) are known to interfere with the staining of the DNA (i.e. fluorescence quenching) and may introduce serious stoichiometric errors (Greilhuber 1987, 2008). The variation in the genome size of Eurasian Valeriana officinalis complex (Capri- foliaceae) has come about by the three described principal mechanisms. The complex thus comprises three major ploidy levels: di-, tetra- and octoploidy (Walther 1949, Titz 1964, 1969). Aneuploidy is indicated by the presence of a B chromosome in tetraploid individuals in an Italian population (Corsi et al. 1984), which contrasts with earlier stud- ies that report solely euploidy for a large number of individuals (Titz & Titz 1979, 1980, 1981). However, karyological studies mostly comprise only single accession or a few individuals per population. Finally, monoploid genome size in di- and octoploid individ- uals indicates elimination of DNA in octoploids (Hidalgo et al. 2010). Complex morphological differentiation is proposed for V. officinalis (Titz & Titz 1979, 1981, 1982, Titz 1984) with ploidy levels corresponding to “basic types”, which are further divided into informal taxa called “types”. Mixed populations consisting of dif- ferent “types” and of morphologically different forms are repeatedly described, resulting in variation being rather continuous and what are now considered as “transitional types” (Keller 1973, Titz & Titz 1979, 1981). Little is known about the evolutionary history and associated mechanisms underlying the differentiation of the V. officinalis complex (for convenience, henceforth the complex will be referred to as V. officinalis), but hybridiza- tion between diploids and polyploids as well as among polyploids is assumed based on morphological evidence (e.g. Titz & Titz 1979,
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