Comparative analyses of stress-induced dynamics in global differential gene expression across more than 550 million years of streptophyte evolution
by Armin Dadras
Date of Examination:2024-10-25
Date of issue:2024-11-22
Advisor:Prof. Dr. Jan de Vries
Referee:Prof. Dr. Jan de Vries
Referee:Prof. Dr. Tim Beißbarth
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http://dx.doi.org/10.53846/goediss-10861
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Abstract
English
The transition from aquatic to terrestrial habitats was a major evolutionary step in the evolution of plants. It ushered in the birth of embryophytes. This transition occurred before the last common ancestor (LCA) of land plants (embryophytes) lived. This land-dwelling LCA of land plants had a diverse range of physiological and developmental features that were adaptive on land, enabling its descendants to inhabit nearly all regions of the Earth. This pivotal moment in the history of evolution poses an important query: what were the essential components enabled this monophyletic group to successfully adapt to terrestrial life? A variety of abiotic stressors that occurred in pronounced severity on land posed a significant obstacle to this transition. Thus, early colonizers of land faced numerous challenges, including osmotic stress, temperature fluctuations, water scarcity, and increased irradiation. Considering their adaptation to terrestrial environments, it is reasonable to believe that the LCA of land plants already had mechanisms in place to detect, communicate, and respond to different environmental cues. Here, we studied living terrestrial plants and their closest algal relatives challenged with various abiotic stress conditions to discover the ancient mechanisms involved. Our objective was to reconstruct the original set of molecular biological tools that facilitated the colonization of land by incorporating a phylogenetic framework into comparative gene expression research. The Zygnematophyceae, which are the closest algal relatives of land plants, belong to a genus of streptophyte algae that has recently gained significant attention. Phylogenetic investigations have significantly improved our understanding of the relationships between the six primary streptophyte algae classes (Zygnematophyceae, Coleochaetophyceae, Charophyceae, Klebsormidiophyceae, Chlorokybophyceae, and Mesostigmatophyceae), as well as their closest cousins, Chlorophytes and Embryophytes. The recent sequencing and annotation of genomes from significant representative streptophyte algae present an exceptional opportunity to investigate the expansion, contraction, and innovation of numerous gene families throughout the course of 550 million years of green lineage evolution. These findings have demonstrated that several genes for characteristics previously believed to be exclusive to land plants were actually already present in their algal ancestors. Prominent instances include phytohormone signaling, communication between plastids and the nucleus, formation of phragmoplasts, synthesis of compounds derived from phenylpropanoids, and routes for responding to stress. However, establishing the presence or absence of gene families merely represents the initial stage. Multiple instances of evolutionary developmental biology (Evo-Devo) have demonstrated that the structure, behaviors, and traits of organisms are influenced by gene regulatory networks and the spatiotemporal control of genes in various environments and developmental stages. In order to determine the preserved patterns of responses to abiotic stressors in land plants and their closest algal relative, it is necessary to examine the gene expression profile. We utilized state-of-art statistical models and bioinformatics techniques to identify stress response patterns that extend across a range of 550 million years of evolutionary history. Based on RNA-Seq datasets generated by our research team, I have re-annotated the genome of Mesotaenium endlicherianum and enhanced the number of predicted protein coding genes by twofold compared to the initial annotation. The annotation's significant improvement was also highlighted by measures such as BUSCO score and Annotation Edit Distance. Expanding on this, I examined the differences in gene expression between different types of streptophyte algae, specifically M. endlicherianum and Zygnema circumcarinatum, and compared them to changes in gene expression in various land plant species, including Physcomitrium patens, Marchantia polymorpha, and Arabidopsis thaliana. In addition, I conducted co-expression network analysis to identify clusters of genes that collaborate in response to diverse abiotic stressors. I then compared the outcomes of this investigation across different phylogenetic clades. I employed Weighted Gene Co-expression Network Analysis (WGCNA) to examine the outcomes of a gradient table of various temperatures and light intensities. In a separate investigation, I employed Dirichlet Process paired with Gaussian process (DPGP) on time series datasets to identify gene clusters by leveraging the temporal relationships within the datasets. For my third research project, I employed a modified version of Graphical Lasso known as Rapid Condition adaptable Fused Graphical Lasso (RCFGL) to reconstruct a sparse but highly robust co-expression network. This was done utilizing publicly accessible datasets for nine different organisms and various abiotic conditions. Furthermore, I employed a combination of Granger causality and Random Forest to predict the gene regulatory network using our time series dataset. By examining the subject from multiple perspectives and employing diverse methodologies, we were able to reconstruct a reliable picture. This was achieved by analyzing expression data spanning 550 million years of evolution in terrestrial plants and their closest algal relative. Our investigation revealed the presence of various mechanisms, including the formation of lipid droplets, genetic signatures of signals derived from plastids and cell walls, osmosensors, kinase signaling, calcium-dependent signaling, and signaling mediated by abscisic acid and ethylene. These mechanisms can be traced back to the last common ancestor of zygnematophyceae and land plants. Furthermore, our data, along with other studies, indicate that the algal ancestor of land plants possessed several genetic elements related to stress perception, signaling, and response, including the ability to respond to auxin, salicylic acid, and jasmonic acid, as well as the biosynthesis of certain specialized metabolites like flavonoids. With the advent of land plants, various modules and gene families were integrated in the LCA of embryophytes, leading to the intricacies in molecular networks that are akin to all plants on land.
Keywords: Plant terrestrialization; Transcriptomics; Streptophyta; Mesotaenium endlicherianum; Zygnema circumcarinatum; Genome annotation; Green lineage; Stress-responsive networks; Evolution; Comparative transcriptomics; Co-expression network analysis; Gene regulatory network inference; Differential gene expression analysis; Algae; Plants
