Genome size diversity in orchids: consequences and evolution

Abstract

Background: The amount of DNA comprising the genome of an organism (its genome size) varies a remarkable 40 000-fold across eukaryotes, yet most groups are characterized by much narrower ranges (e.g. 14-fold in gymnosperms, 3- to 4-fold in mammals). Angiosperms stand out as one of the most variable groups with genome sizes varying nearly 2000-fold. Nevertheless within angiosperms the majority of families are characterized by genomes which are small and vary little. Species with large genomes are mostly restricted to a few monocots families including Orchidaceae.

Scope: A survey of the literature revealed that genome size data for Orchidaceae are comparatively rare representing just 327 species. Nevertheless they reveal that Orchidaceae are currently the most variable angiosperm family with genome sizes ranging 168-fold (1C = 0.33-55.4 pg). Analysing the data provided insights into the distribution, evolution and possible consequences to the plant of this genome size diversity.

Conclusions: Superimposing the data onto the increasingly robust phylogenetic tree of Orchidaceae revealed how different subfamilies were characterized by distinct genome size profiles. Epidendroideae possessed the greatest range of genome sizes, although the majority of species had small genomes. In contrast, the largest genomes were found in subfamilies Cypripedioideae and Vanilloideae. Genome size evolution within this subfamily was analysed as this is the only one with reasonable representation of data. This approach highlighted striking differences in genome size and karyotype evolution between the closely related Cypripedium, Paphiopedilum and Phragmipedium. As to the consequences of genome size diversity, various studies revealed that this has both practical (e.g. application of genetic fingerprinting techniques) and biological consequences (e.g. affecting where and when an orchid may grow) and emphasizes the importance of obtaining further genome size data given the considerable phylogenetic gaps which have been highlighted by the current study.

Fig. 1.

Distribution of genome sizes (1C-values) for 327 species of Orchidaceae.

Fig. 2.

(A) Relationship between the five orchid subfamilies (left, based on data in Chase et al., 2003) and 1C-value data (right) showing the mean (filled circles) followed by the range of nuclear DNA C-values for each subfamily. The number in brackets following the subfamily name corresponds to the percentage of species with genome size data. (B–E) Histograms showing the distribution of C-values in each subfamily.

Fig. 3.

A phylogenetic tree showing the major subdivisions of Orchidaceae (subfamilies, tribes and subtribes) based on Chase et al. (2003). Taxonomic groups with at least one genome size estimate are shown in bold. * Epid. = Epidendreae, Podo. = Podochileae, Areth. = Arethuseae.

Fig. 4.

(A) Part of informative AFLP traces for Liparis loeselii (1C = 6·8 pg) with two variable bands indicated by arrows. (B) An extreme case of uninformative AFLP traces for two representative individuals of Cypripedium calceolus (1C = 32·4 pg) and one individual of C. macranthos (1C = 37·4 pg). In this case, the only interpretable band was present in all samples of C. calceolus and in C. macranthos and was therefore of no utility in population genetics.

Fig. 5.

The relationship between 1C DNA amount and minimum duration of meiosis in 20 angiosperm species. Arrows mark estimated duration of meiosis for (A) Trichocentrum maduroi (1C = 0·33 pg) and (B) Pogonia ophioglossoides (1C = 55·4 pg). Graph redrawn from data given in Bennett (1977).

Fig. 6.

The distribution of 1C DNA amounts in (A) terrestrial and (B) epiphytic orchids.

Fig. 7.

The range of genome sizes and chromosome numbers encountered in four of the five genera comprising subfamily Cypripedioideae. The phylogenetic framework is based on Cox et al. (1997a), and chromosome data are taken from Brandham (1999).

Fig. 8.

Mitotic chromosome preparations of (A) Phragmipedium besseae (1C = 7·1 pg) and (B) Mexipedium xerophyticum (1C = 6·7 pg), both taken at the same magnification to show the broad similarity in chromosome size, and hence genome size between the two species. (C) Paphiopedilum parishii (2n = 26 comprising all metacentric chromosomes) and (D) P. bullenianum (2n = 40 comprising 12 metacentric and 28 telocentric chromosomes. (E) Cypripedium molle (1C = 4·1 pg) and (F) C. calceolus (1C = 32·4 pg) at the same magnification. Both species have 2n = 20 so the differences in chromosome size reflect the approx. 8-fold difference in genome size. Scale bars = 10 µm. The image in (B) was taken from Cox et al. (1997b) and reprinted with permission from Lindleyana. Images (C) and (D) were taken from Karasawa (1979) and reproduced with permission from the Bulletin of the Hiroshima Botanic Garden.

Fig. 9.

(A) Genome size data for 22 species of Paphiopedilum superimposed onto a framework showing the phylogenetic relationships of Paphiopedilum species. (B) The relationship between chromosome number and genome size in Paphiopedilum. Both figures are redrawn and modified from Cox et al. (1998).