Diversification in the genetic architecture of gene expression and transcriptional networks in organ differentiation of Populus

Abstract

A fundamental goal of systems biology is to identify genetic elements that contribute to complex phenotypes and to understand how they interact in networks predictive of system response to genetic variation. Few studies in plants have developed such networks, and none have examined their conservation among functionally specialized organs. Here we used genetical genomics in an interspecific hybrid population of the model hardwood plant Populus to uncover transcriptional networks in xylem, leaves, and roots. Pleiotropic eQTL hotspots were detected and used to construct coexpression networks a posteriori, for which regulators were predicted based on cis-acting expression regulation. Networks were shown to be enriched for groups of genes that function in biologically coherent processes and for cis-acting promoter motifs with known roles in regulating common groups of genes. When contrasted among xylem, leaves, and roots, transcriptional networks were frequently conserved in composition, but almost invariably regulated by different loci. Similarly, the genetic architecture of gene expression regulation is highly diversified among plant organs, with less than one-third of genes with eQTL detected in two organs being regulated by the same locus. However, colocalization in eQTL position increases to 50% when they are detected in all three organs, suggesting conservation in the genetic regulation is a function of ubiquitous expression. Genes conserved in their genetic regulation among all organs are primarily cis regulated (approximately 92%), whereas genes with eQTL in only one organ are largely trans regulated. Trans-acting regulation may therefore be the primary driver of differentiation in function between plant organs.

Fig. 1.

Global distribution of eQTL across linkage groups for (A) xylem, (B) leaf, and (C) root tissues expressed as the fraction of mapped gene models. In cases where values on the eQTL/mapped genes axis exceed 70, values are provided in brackets. See Table S1 footnotes for description of cis- and trans-eQTL categorization procedure.

Fig. 2.

Overlap between genes and eQTL detected among the three tissues considered. (A) Overlap of genes producing eQTL in each of the three tissues, including genes with physical position undefined in the genome. (B) Cross-tissue conservation of the genomic regulatory region (eQTL location) detected for genes in A. (C) Cross-tissue conservation of genomic regulatory position for genes with cis-eQTL. (D) Cross-tissue conservation of genomic regulatory position for genes with trans-eQTL. Genes in unknown position (ambiguous) in the genome are excluded.

Fig. 3.

Genome-wide linkage scan of expression traits and demarcation of eQTL hotspots containing coexpressed gene networks in leaf tissue. Similar results were obtained for root and xylem tissue, detailed in Table 1.

Fig. 4.

Leaf coexpression network constructed from the “blue” eQTL hotspot and enriched for chloroplast-related Gene Ontogeny categories. Hub colors indicate annotation nature of network members, and edges indicate Pearson correlation between coexpressed genes of |r| > 0.80.