Reshaping of the maize transcriptome by domestication

Abstract

Through domestication, humans have substantially altered the morphology of Zea mays ssp. parviglumis (teosinte) into the currently recognizable maize. This system serves as a model for studying adaptation, genome evolution, and the genetics and evolution of complex traits. To examine how domestication has reshaped the transcriptome of maize seedlings, we used expression profiling of 18,242 genes for 38 diverse maize genotypes and 24 teosinte genotypes. We detected evidence for more than 600 genes having significantly different expression levels in maize compared with teosinte. Moreover, more than 1,100 genes showed significantly altered coexpression profiles, reflective of substantial rewiring of the transcriptome since domestication. The genes with altered expression show a significant enrichment for genes previously identified through population genetic analyses as likely targets of selection during maize domestication and improvement; 46 genes previously identified as putative targets of selection also exhibit altered expression levels and coexpression relationships. We also identified 45 genes with altered, primarily higher, expression in inbred relative to outcrossed teosinte. These genes are enriched for functions related to biotic stress and may reflect responses to the effects of inbreeding. This study not only documents alterations in the maize transcriptome following domestication, identifying several genes that may have contributed to the evolution of maize, but highlights the complementary information that can be gained by combining gene expression with population genetic analyses.

Fig. 1.

Variance in expression. (A) Density plots for the coefficient of variance (CoVar) for gene expression levels in all genotypes (black), maize genotypes (red), and teosinte genotypes (blue), as well as for developmental stages (green). More genes exhibit a higher CoVar across developmental stages than across diverse genotypes. (B) Relative gene expression levels for the 612 genes with significant expression differences between maize and teosinte, and used for hierarchical clustering. Genotypes were each assigned to one of five subpopulations (specified in Table S1). (C) Similar clustering is shown for the 45 genes that are differentially expressed between inbred and outcrossed teosinte. NSS (nonstiff stalk); SS (stiff stalk).

Fig. 2.

Rewiring of transcriptional networks in maize and teosinte. (A) Pearson correlation coefficient was determined for the full matrix correlation of maize and teosinte coexpression networks (black arrow). Only 1.4% of 1,000 pairs of networks derived from randomly permuting the genotypes exhibit lower correlations than the maize and teosinte networks. (B) Scatterplot shows the correlation between all gene pairs in maize (x axis) relative to the correlation for the same gene pair in teosinte (y axis). The relative density of data points in B was compared with the average for 1,000 bootstrap coexpression networks in C. Blue regions indicate fewer observed correlations relative to the bootstrap networks, whereas red coloration indicates an excess of actual observations, providing evidence for an enrichment of gene pairs with varying correlations in maize and teosinte.

Fig. 3.

Analysis of genes with altered expression or conservation and targets of selection during improvement and/or domestication. (A) Venn diagram showing the overlap between DE genes, AEC genes, and the genes that occur in genomic regions that have evidence for selective sweeps during maize domestication or improvement (Dom/Imp genes). (B) Teosinte coexpression networks for three genes (GRMZM2G068436, GRMZM2G137947, and GRMZM2G375302). (Right) Edges that are maintained in maize coexpression networks are shown. Although the differentially expressed gene (red node) is highly connected in teosinte, most of these connections are lost in maize. However, some parts of the teosinte network are still conserved in maize. (C) Cross-population composite likelihood ratio test (XP-CLR) plot shows the evidence for a selective sweep that occurs on chromosome 9. The tick marks along the x axis represent genes, and the red tick mark indicates the gene (GRMZM2G448355) that was chosen as the candidate target of selection and is differentially expressed in maize and teosinte. The bar plot underneath the graph shows the expression levels of all maize (blue) and teosinte (red) samples. (D) XP-CLR plot for a large region on chromosome 5. The candidate target of selection is indicated in green and shows similar expression in maize and teosinte. Two other genes (red) exhibit DE. (E) Neighbor-joining tree shows the relationships among the haplotypes at GRMZM2G141858. (Right) Bar plot shows expression levels for each genotype; red bars indicate teosinte genotypes, and blue bars represent maize genotypes. At least one teosinte genotype (TIL15) contains the haplotype that has been selected in maize and has expression levels similar to maize genotypes.