Comparative analysis of the transcriptomes of Populus trichocarpa and Arabidopsis thaliana suggests extensive evolution of gene expression regulation in angiosperms

Abstract

Summary• Sequencing of the Populus trichocarpa genome creates an opportunity to describe the transcriptome of a woody perennial species and establish an atlas of gene expression. A comparison with the transcriptomes of other species can also define genes that are conserved or diverging in plant species.• Here, the transcriptome in vegetative organs of the P. trichocarpa reference genotype Nisqually-1 was characterized. A comparison with Arabidopsis thaliana orthologs was used to distinguish gene functional categories that may be evolving differently in a woody perennial and an annual herbaceous species.• A core set of genes expressed in common among vegetative organs was detected, as well as organ-specific genes. Statistical tests identified chromatin domains, where adjacent genes were expressed more frequently than expected by chance. Extensive divergence was detected in the expression patterns of A. thaliana and P. trichocarpa orthologs, but transcription of a small number of genes appeared to have remained conserved in the two species.• Despite separation of lineages for over 100 million yr, these results suggest that selection has limited transcriptional divergence of genes associated with some essential functions in A. thaliana and P. trichocarpa. However, extensive remodeling of transcriptional networks indicates that expression regulation may be a key determinant of plant diversity.

Contrasting patterns of evolution following whole genome versus tandem duplication events inPopulus

“…However, broadly expressed (i.e., combined breadth above 80%) gene pairs did have a significant nonlinear relationship between expression distance and d N /d S . Previous studies in Populus revealed that more broadly expressed genes tend to be predominantly cis regulated, while trans regulation drives more tissue-specific expression (Quesada et al 2008;Drost et al 2010), a finding that is broadly consistent with our results. Our data further suggest that expression divergence in broadly expressed genes may be reflected in coding sequence polymorphisms as well as variation in cis regulatory domains in noncoding regions.…”

The Cytokinin Type-B Response Regulator PtRR13 Is a Negative Regulator of Adventitious Root Development inPopulus

“…RNA extracted from these samples was used for microarray analyses with a custom-designed NimbleGen array containing features representing 55,793 annotated gene models from the sequenced genome of Populus trichocarpa, including 45,555 predicted gene models reported previously (Tuskan et al, 2006) plus an additional 10,238 gene models showing evidence of transcription (Quesada et al, 2008). Transcripts showing significant differences in abundance at a false discovery rate (FDR; Storey and Tibshirani, 2003) of 5% between adjacent time points (0-6 h, 6-24 h, and 24-48 h) were identified.…”

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

“…In primates, mutations that diversify the transcriptional regulation of genes expressed in multiple organs are more likely to be eliminated by negative selection (21). Similarly, orthologs expressed in multiple compartments in Arabidopsis and Populus are more likely to be expressed at similar levels, compared with genes that are specific to a single tissue or organ in both species (22). An extension of these observations would suggest that for genes in which eQTL are detected in multiple organs, the genetic regulation may be more conserved compared with those that are organ specific, which could evolve more rapidly by establishing alternative, trans-acting genetic mechanisms of regulation.…”