The Amount of Nitrogen Used for Photosynthesis Modulates Molecular Evolution in Plants

Abstract

Genome and transcript sequences are composed of long strings of nucleotide monomers (A, C, G, and T/U) that require different quantities of nitrogen atoms for biosynthesis. Here, it is shown that the strength of selection acting on transcript nitrogen content is influenced by the amount of nitrogen plants require to conduct photosynthesis. Specifically, plants that require more nitrogen to conduct photosynthesis experience stronger selection on transcript sequences to use synonymous codons that cost less nitrogen to biosynthesize. It is further shown that the strength of selection acting on transcript nitrogen cost constrains molecular sequence evolution such that genes experiencing stronger selection evolve at a slower rate. Together these findings reveal that the plant molecular clock is set by photosynthetic efficiency, and provide a mechanistic explanation for changes in plant speciation rates that occur concomitant with improvements in photosynthetic efficiency and changes in the environment such as light, temperature, and atmospheric CO2 concentration.

Physicochemical Foundations of Life that Direct Evolution: Chance and Natural Selection are not Evolutionary Driving Forces

“…Accordingly, plant genomes and proteomes are AT-rich and contain amino acids that require fewer nitrogen atoms as compared with animal genomes and proteomes. This fits well with the fact that nitrogen sources are limited for plants, while animals can access organic sources of nitrogen [23,36,37]. Of note, in eukaryotic genes containing introns, exons and introns have the same composition bias [79].…”

“…As for proteins, environmental physicochemical parameters (temperature and chemical composition) constrain the nucleotide composition of genomes and this can be observed in thermophilic, halophilic, acidophilic, aerobic, and radiation-exposed organisms [28,35]. Finally, the amount of DNA per cell (genome size and ploidy) is constrained by the environmental availability of phosphorus, and the genomes of organisms growing in a nitrogen-poor environment are enriched in A:T pairs, which require seven nitrogens instead of the eight used in G:C pairs [36][37][38].…”

“…Along the same line, the organization of the genetic code allows nucleic and amino acid polymers to co-adapt to the bioavailability of nitrogen. Indeed, A:T pairs require fewer nitrogen atoms than G:C pairs (7 vs. 8, respectively) and correspond to amino acids that also require fewer nitrogen atoms [23,36,37]. Accordingly, plant genomes and proteomes are AT-rich and contain amino acids that require fewer nitrogen atoms as compared with animal genomes and proteomes.…”

A Novel Hypothesis for the Role of Photosynthetic Physiology in Shaping Macroevolutionary Patterns

“…Apart from the ecophysiological significance of angiosperms' higher PNUE (Lusk et al, 2003), recent evidence has also suggested a strong link between PNUE and the rate of molecular evolution. Kelly (2018) showed that species that overinvest in N for their photosynthetic enzymes (i.e. gymnosperms in our study with high V Cmax, 20°C values; Supplemental Table S2) evolve slowly, while species that reduced N investment (i.e.…”

Genome-wide identification, phylogeny, and expression profiling of RWP-RK gene family under low nitrogen and nodulation in Arabidopsis and legumes

“…To biosynthesize the precursors of these biomacromolecules, plants must integrate inorganic carbon (CO 2 ) and nitrogen (NO 3 − /NH 4 + ); however, compared to CO 2 , NO 3 − /NH 4 + is more difficult to obtain from the environment. Therefore, plant growth is generally nitrogen limited in both natural and agricultural environments [46]. The extensive use of synthetic fertilizers in developed countries is expensive and environmentally damaging.…”