Stoichiometry versus ecology: the relationships between genome size and guanine-cytosine content, and tissue nitrogen and phosphorus in grassland herbs

Abstract

Background and aims: Plant tissue nitrogen (N) and phosphorus (P) and genome traits, such as genome size and guanine-cytosine (GC) content, scale with growth or metabolic rates and are linked to plant ecological strategy spectra. Tissue NP stoichiometry and genome traits are reported to affect plant growth, metabolic rates or ecological strategies in contrasting ways, although the elemental costs for building and maintaining DNA are typically overlooked.

Methods: We formulated stoichiometry- and ecology-based predictions on the relationship between genome size and GC content to tissue N, P and N : P and tested them on a set of 130 herbaceous species from a temperate grassland using ordinary, phylogenetic and quantile regression.

Key results: Genome size was only negatively linked to plant N and N : P in species with very small genomes. We found no link between genome size and plant P. GC content was negatively linked to plant N and P but we found these significant links consistently in both GC-rich and GC-poor species. Finally, GC content correlated positively with plant N : P but only in species with GC-rich genomes.

Conclusions: Our results provide stronger support for the ecology-based predictions than the stoichiometry-based predictions, and for the links between GC content and plant N and P stoichiometry than for genome size. We argue that the theories of plant metabolic rates and ecological strategies (resource-acquisitive vs. conservative or ruderal vs. stress-tolerator spectra) better explain interspecific genome-NP stoichiometry relationships at the tissue level (although relatively weakly) than the stoichiometric theory based on the elemental costs for building and maintaining DNA.

Keywords: GC content; genome size; nitrogen; phosphorus; plant ecological strategies; stoichiogenomics; tissue stoichiometry.

Fig. 1.

The stoichiometry-based and ecology-based perspectives (Table 1) often suggest contradicting predictions of the relationships between plant genome size (1C or 1Cx value), guanine–cytosine (GC) content, and plant tissue nitrogen (N), phosphorus (P), and N : P ratio. Black lines indicate hypothesized trends for the central tendencies, whereas grey lines indicate hypothesized trends in lower, middle and upper quantiles. (A) DNA is an N- and P-demanding biomolecule, and thus its content (1C value) can be positively correlated with plant tissue N and P, while it can be negatively linked to plant N : P because DNA is a relatively P-rich biomolecule with low N : P. The stoichiometry-based perspective also predicts positive links of GC content to plant N and N : P, because GC pairs have more N atoms in their molecules than AT pairs. We also expected that the proposed relationships would be more pronounced in upper quantiles, i.e. in plants with large genomes and GC-rich nucleotide compositions that can contribute more to the overall plant N and P pools than small genomes or GC-poor nucleotide compositions. (B) The ecology-based perspective suggests negative links of genome size to plant N and P and a positive link to N : P. Stress-tolerant species are typically slowly growing and conservative, with larger genomes but lower N and P, and higher N : P compared to fast-growing and acquisitive ruderals. Ecological strategies are also connected to GC content as P-poor (but with high tissue N : P) stress tolerators tend to have higher GC content. The strength of the proposed relationships can vary across quantiles; for example, small genome species (lower quantiles) might allocate more P and N to RNA and proteins, respectively, to promote fast growth.

Fig. 2.

Relationships of (A–C) genome size (1C value) and (D–F) guanine–cytosine (GC) content to plant tissue nitrogen (N), phosphorus (P) and N : P ratio across quantiles. Only significant quantiles (q) are shown (P < 0.05, Table 3). Genome size is ln-transformed.