Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation

Abstract

Summary Angiosperm genome sizes (GS) range c. 2400‐fold, and as nucleic acids are amongst the most phosphorus‐ (P) and nitrogen (N)‐demanding cellular biomolecules, we test the hypothesis that a key influence on plant biomass and species composition is the interaction between N and P availability and plant GS.We analysed the impact of different nutrient regimes on above‐ground biomass of angiosperm species with different GS, ploidy level and Grime's C‐S‐R (competitive, stress‐tolerant, ruderal) plant strategies growing at the Park Grass Experiment (Rothamsted, UK), established in 1856.The biomass‐weighted mean GS of species growing on plots with the addition of both N and P fertilizer were significantly higher than that of plants growing on control plots and plots with either N or P. The plants on these N + P plots are dominated by polyploids with large GS and a competitive plant strategy.The results are consistent with our hypothesis that large genomes are costly to build and maintain under N and P limitation. Hence GS and ploidy are significant traits affecting biomass growth under different nutrient regimes, influencing plant community composition and ecosystem dynamics. We propose that GS is a critical factor needed in models that bridge the knowledge gap between biodiversity and ecosystem functioning.

Impacts of Nitrogen and Phosphorus: From Genomes to Natural Ecosystems and Agriculture

“…Recent evidence suggests that genome structure (i.e., genome size, ploidal level) and nutrient availability can influence plant distributions, community composition, and biomass production in grasslands (Šmarda et al, 2013;Guignard et al, 2016;Segraves, 2017). This possibility is bolstered by large-scale comparative analyses using the Plant DNA C-values database (Bennett and Leitch, 2012) which suggest that plants with large genomes are at greater risk of extinction and are less tolerant of polluted soils and extreme environmental conditions (Vinogradov, 2003;Knight et al, 2005;Greilhuber and Leitch, 2013).…”

“…Support for these predictions has come from recent studies of freshwater snails (Neiman et al, 2013b) and angiosperms (Šmarda et al, 2013;Guignard et al, 2016). Further data collection on, and empirical tests of, the associations between N and P limitation, genome size, and ploidal-level variation in diverse habitat types and biomes are clearly needed to determine how far such predictions hold across different ecosystems and larger, continental scales.…”

“…At the organism level, N and P availability is known to have powerful influences on functional traits and growth rates, but we are only just beginning to understand that genome structure (e.g., genome size, ploidal level) can also play an important role (e.g., Neiman et al, 2009Neiman et al, , 2013bŠmarda et al, 2013;Guignard et al, 2016). At the genomic level, environmental nutrient limitation may constrain cellular processes (e.g., photosynthesis, transcriptomes) and over time may result in divergence of genes and the proteins they encode (Acquisti et al, 2009a,b;Elser et al, 2011;Seward and Kelly, 2016; Figure 1).…”

Ploidy‐altered phenotype interacts with local environment and may enhance polyploid establishment in Knautia serpentinicola (Caprifoliaceae)

“…Chao et al ., ) suggesting higher nutrient‐uptake efficiency of polyploids when compared to diploids. Also, a long‐term application of phosphorus to oligotrophic grasslands substantially increased the relative success of polyploids at particular sites (Šmarda et al ., ; Guignard et al ., ). On the other hand, diploid and tetraploid Dactylis glomerata from a primary contact zone did not show significant differences in cytotype performance when cultivated in either fertilised or nonfertilised substrate (Bretagnolle & Thompson, ).…”

Interspecific variation in ploidy as a key plant trait outlining local extinction risks and community patterns in fragmented landscapes

“…Diploid plant species are overrepresented among threatened species worldwide (Pandit, Pocock, & Kunin, ), suggesting that ploidy may be linked to species extinction risks and therefore differential diversity losses and plant community dynamics (Guignard et al., ; Šmarda et al., ). Hence, we hypothesize that interspecific variation in ploidy may influence plant species distributions and community composition in fragmented landscapes, over ecological time‐scales (Lumaret, Guillerm, Maillet, & Verlaque, ; Rosche et al., ).…”