Plant organ evolution revealed by phylotranscriptomics in Arabidopsis thaliana

Abstract

The evolution of phenotypes occurs through changes both in protein sequence and gene expression levels. Though much of plant morphological evolution can be explained by changes in gene expression, examining its evolution has challenges. To gain a new perspective on organ evolution in plants, we applied a phylotranscriptomics approach. We combined a phylostratigraphic approach with gene expression based on the strand-specific RNA-seq data from seedling, floral bud, and root of 19 Arabidopsis thaliana accessions to examine the age and sequence divergence of transcriptomes from these organs and how they adapted over time. Our results indicate that, among the sense and antisense transcriptomes of these organs, the sense transcriptomes of seedlings are the evolutionarily oldest across all accessions and are the most conserved in amino acid sequence for most accessions. In contrast, among the sense transcriptomes from these same organs, those from floral bud are evolutionarily youngest and least conserved in sequence for most accessions. Different organs have adaptive peaks at different stages in their evolutionary history; however, all three show a common adaptive signal from the Magnoliophyta to Brassicale stage. Our research highlights how phylotranscriptomic analyses can be used to trace organ evolution in the deep history of plant species.

Phylostratigraphic Analysis Shows the Earliest Origination of the Abiotic Stress Associated Genes in A. thaliana

“…Among them, very rarely (only two cases) are genes subject to positive Darwinian selection (DI > 1), which is very small compared to the proportion of such genes in the entire genome. This is generally consistent with data from Lei et al, according to which A. thaliana genes of DI > 1 are enriched in lipid localization, transport and binding, and the endomembrane system (i.e., stress unrelated terms) [37]. However, it should be noted that the use of the genome pair A. thaliana vs. A. lyrata for DI estimates (i.e., Ka/Ks) might provide insight into genes that evolved under different selection regimes only in the most recent past.…”

“…The values of the DI close to 0 indicate strong purifying selection acting on a gene. The DI measure is often used to estimate the level of the selective pressure on the transcriptomes in phylostratigraphic transcriptome analysis [24,[35][36][37][38].…”

myTAI: evolutionary transcriptomics with R

“…We recently used myTAI to investigate the developmental hourglass model of embryo development ( Raff, 1996 ) on the transcriptomic level ( Quint et al , 2012 ; Drost et al , 2017 ). Others used myTAI to investigate transcriptome conservation in plant organ development ( Lei et al , 2017 ). To illustrate an example workflow with myTAI , we here use the developmental transcriptome of Arabidopsis thaliana embryo development ( Quint et al , 2012 ) (see Supplementary Material for more details about data formats):…”

Foster thy young: Enhanced prediction of orphan genes in assembled genomes

“…A subset of orphans are retained in the genome and continue to evolve, such that each genome contains a mixture of genes of different ages (phylostrata) 1,3 . Phylostratigraphic analyses 3 indicates orphans played a role in development of new reproductive and neural structures across evolutionary time [29][30][31] . Thus, the advent of new genes may provide a critical enabler of speciation.…”

“…Some proteins encoded by orphan genes (e.g., toxins 6 ) act externally, while others integrate into internal metabolic and developmental pathways 7 . Phylostratigraphic reconstructions have implicated orphans in the evolution of new reproductive and neural structures 10,11 . Thus, the advent of orphan genes may provide a critical enabler of speciation.…”