Ecological nitrogen limitation shapes the DNA composition of plant genomes

Abstract

Phenotypes and behaviors respond to resource constraints via adaptation, but the influence of ecological limitations on the composition of eukaryotic genomes is still unclear. We trace connections between plant ecology and genomes through their elemental composition. Inorganic sources of nitrogen (N) are severely limiting to plants in natural ecosystems. This constraint would favor the use of N-poor nucleotides in plant genomes. We show that the transcribed segments of undomesticated plant genomes are the most N poor, with genomes and proteomes bearing signatures of N limitation. Consistent with the predictions of natural selection for N conservation, the precursors of transcriptome show the greatest deviations from Chargaff's second parity rule. Furthermore, crops show higher N contents than undomesticated plants, likely due to the relaxation of natural selection owing to the use of N-rich fertilizers. These findings indicate a fundamental role of N limitation in the evolution of plant genomes, and they link the genomes with the ecosystem context within which biota evolve.

FIG. 1.—

Patterns of N content in the DNA sequences of plant and animal genomes. The N contents for the transcriptome (histogram) and the whole genome are shown for a plant (A) and two animals (B). The mean and standard deviation (SD) of the transcriptomic N content derived from introns are given in table 1. Distributions of the deviations from Chargaff's second parity rule (difference between the N contents of the sense and antisense strands in introns) are shown in (C). The mean, SD, and standard error (respectively) for the deviations from Chargaff's second parity rule are Arabidopsis thaliana (−0.352, 0.226, and 0.001), Drosophila melanogaster (0.090, 0.191, and 0.001), and Homo sapiens (−0.058, 0.118, and 0.0007).

FIG. 2.—

N contents in the genome, transcriptome and proteome of undomesticated and crop species. (A) Distribution of N content in the transcriptomes and (B) deviations from Chargaff's second parity rule in Arabidopsis thaliana (undomesticated) and Oryza sativa (crop). The mean, SD, standard error (SE), and sample size (number of genes) of N content distribution in (A) are A. thaliana (3.485, 0.114, 0.0007, and 26,544) and O. sativa (3.616, 0.139, 0.0006, and 54,712). The overall genomic N content was 3.680 (119 × 10⁶ bp) for A. thaliana and 3.718 (372 × 10⁶ bp) for O. sativa. In (B), the mean, SD, and SE of the difference between the N contents of the sense and antisense strands are −0.352, 0.226, and 0.001 for A. thaliana, and −0.171, 0.249, and 0.001 for O. sativa, with the whole-genome deviation close to zero in both species (A. thaliana = 0.0008 and O. sativa = 0.0002). (C) N content per amino acid side chain of protein sequences in crops plants known to be symbiotically related to N-fixing bacteria, undomesticated plants, and animals. The mean, SD, and the sample size (number of amino acids and proteins) for each species are shown on the right.