Evolution of DNA amounts across land plants (embryophyta)

Abstract

Background and aims: DNA C-values in land plants (comprising bryophytes, lycophytes, monilophytes, gymnosperms and angiosperms) vary approximately 1000-fold from approx. 0.11 to 127.4 pg. To understand the evolutionary significance of this huge variation it is essential to evaluate the phylogenetic component. Recent increases in C-value data (e.g. Plant DNA C-values database; release 2.0, January 2003; http://www.rbgkew.org.uk/cval/homepage.html) together with improved consensus of relationships between and within land plant groups makes such an analysis timely.

Methods: Insights into the distribution of C-values in each group of land plants were gained by superimposing available C-value data (4119 angiosperms, 181 gymnosperms, 63 monilophytes, 4 lycophytes and 171 bryophytes) onto phylogenetic trees. To enable ancestral C-values to be reconstructed for clades within land plants, character-state mapping with parsimony and MacClade was also applied.

Key results and conclusions: Different land plant groups are characterized by different C-value profiles, distribution of C-values and ancestral C-values. For example, the large ( approximately 1000-fold) range yet strongly skewed distribution of C-values in angiosperms contrasts with the very narrow 12-fold range in bryophytes. Further, character-state mapping showed that the ancestral genome sizes of both angiosperms and bryophytes were reconstructed as very small (i.e. < or =1.4 pg) whereas gymnosperms and most branches of monilophytes were reconstructed with intermediate C-values (i.e. >3.5, <14.0 pg). More in-depth analyses provided evidence for several independent increases and decreases in C-values; for example, decreases in Gnetaceae (Gymnosperms) and heterosperous water ferns (monilophytes); increases in Santalales and some monocots (both angiosperms), Pinaceae, Sciadopityaceae and Cephalotaxaceae (Gymnosperms) and possibly in the Psilotaceae + Ophioglossaceae clade (monilophytes). Thus, in agreement with several focused studies within angiosperm families and genera showing that C-values may both increase and decrease, it is apparent that this dynamic pattern of genome size evolution is repeated on a broad scale across land plants.

Fig. 1.

Land plant phylogeny (left; based on Pryer et al., 2001) and C-value data (middle) showing the mean (•) followed by the range of nuclear DNA C-values encountered in each group. The number in brackets following the group name gives the number of species with C-value data. Land plants and their major subdivisions are shown on the right.

Fig. 2.

Histograms showing the distribution of DNA C-values for (A) 4119 angiosperms, (B) 181 gymnosperms, (C) 63 monilophytes, (D) 4 lycophytes, and (E) 171 bryophytes. The maximum C-value for each group is indicated.

Fig. 3.

Molecular phylogeny (left) and C-value data (middle) showing the mean (•) followed by the range of nuclear DNA C-values encountered in each group or family of (A) angiosperms, (B) gymnosperms, (C) monilophytes and lycophytes, and (D) bryophytes. The number in brackets following the group or family name gives the number of species with C-value data. Major subdivisions within the angiosperms are shown on the right. Phylogenetic trees taken from the following sources: angiosperms, APG II (2003); gymnosperms, Soltis et al. (2002); monilophytes and lycophytes, Pryer et al. (2001); bryophytes, Beckert et al. (1999).

Fig. 4.

Parsimony reconstruction of C-value diversification in the angiosperms using the ‘all most-parsimonious states’ resolving option of MacClade (based on Soltis et al., 2003). Sant = Santalales.

Fig. 5.

Parsimony reconstruction of C-value diversification in the monocots using the ‘all most-parsimonious states’ resolving option of MacClade (based on Soltis et al., 2003). Families containing species with very large C-values (i.e. ≥35·0 pg) are marked in bold.

Fig. 6.

Distribution of DNA C-values for 62 species of Santalales. The C-values for two Viscum species are arrowed. Data taken from the Plant DNA C-values database (Bennett and Leitch, 2003).

Fig. 7.

Parsimony reconstruction of C-value diversification across land plants using the ‘all most-parsimonious states’ resolving option of MacClade. Equisetum 1 and 2 = Equisetum subgenus Equisetum and subgenus Hippochaete, respectively. ANGIOS. = angiosperms; LYCO. = lycophytes; BRYO. = bryophytes.

Fig. 8.

Parsimony reconstruction of C-value diversification across land plants using the ACCTRAN option of MacClade. Equisetum 1 and 2 = Equisetum subgenus Equisetum and subgenus Hippochaete, respectively. ANGIOS. = angiosperms; LYCO. = lycophytes; BRYO. = bryophytes.