CarotPhyte: Exploring the evolutionary roots for the biosynthesis of apocarotenoids and their role as signals in plastid-mediated stress response in streptophyte algae
by Tim Philipp Rieseberg
Date of Examination:2024-04-16
Date of issue:2024-10-18
Advisor:Prof. Dr. Jan de Vries
Referee:Prof. Dr. Jan de Vries
Referee:Prof. Dr. Ivo Feußner
Persistent Address:
http://dx.doi.org/10.53846/goediss-10806
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Abstract
English
Plant terrestrialization came with enormous multidimensional consequences that shaped planet earth. This terraforming event that occurred about 550 MYA goes back to a single progenitor. Elucidating important facilitators of this singularity is the focus of this thesis. Taking the huge step from water to land comes with severe changes in environmental biotic and abiotic interactions. This conquest of the green lineage was only possible with the adequate molecular toolkit to overcome the challenges terrestrial habitats bear. Thus, pieces of the toolkit that still enables terrestrial lifestyles today must have been present in the last common ancestor of all land plants and originating from the same genetic chassis also in the last common ancestor of Zygnematophyceae and land plants. One of these shared features is the name-giving phragmoplast of the monophylum of Phragmoplastophyta. Charophyceae diverged at the base of this monophylum and harbor complex body plans presumably inheriting features that predated plant terrestrialization but were lost in the sister lineage of all land plants – the Zygnematophyceae – by reductive evolution. To shed light on the different trajectories of Phragmoplastophyta that paved the way to the conquest of land was the aim of this thesis. To do so Charophyceae, Zygnematophyceae, and the model moss Physcomitrium patens were investigated in a comparative fashion. The abiotic hurdles of terrestrial habitats compared to an aquatic lifestyle are quite obvious since essential factors for photosynthetic organisms including water availability, light, and temperature change drastically in quality as well as amplitude and frequency of oscillation. Applying these stressors in controlled lab setups is ideal for testing the functions and conservation of oxidative stress response networks. Additionally, physical conditions change but they do not evolve compared to biotic interactions, and often similar oxidative stress response networks are used. Respecting these oscillations, one line of research of this work focused on the kinetics of these oxidative stress response networks in time-series experiments. This way it was possible to show that many essential molecular machineries of land plant biology did not only predate terrestrialization but that also their dynamic regulation is largely conserved with important differences in Zygnema circumcarinatum heat stress response. These included less regulation by otherwise conserved HSP70–HSP90 (HSP, heat shock protein) organizing protein 3 (HOP3), a stronger morphological response and a smaller and less size-responsive pigment pool. The second approach investigated lineage- and species-specific molecular tool kits under steady-state conditions to dissect the divergence of molecular tools fulfilling similar purposes in streptophyte algae and land plants. The responses of photosynthetic organisms towards altered conditions are well orchestrated on multiple levels of biology including morphology, photophysiology, transcription, and specialized metabolisms. To aptly reflect this, for all studies of this thesis comparative multiangle approaches were chosen including a minimum of two organisms and integrating a minimum of three of the following techniques: Morphological investigations, photophysiology measurements, transcriptomics, and metabolite profiling of intertwined pathways. Two intertwined core pathways of oxidative stress mitigation that presumably were crucial for plant terrestrialization are the carotenoid and the apocarotenoid pathway. Despite their importance, they are largely understudied in streptophyte algae and mosses. This knowledge gap was addressed by this work. Major conservation in Phragmoplastophyta and land plants of flux responses and the surrounding genetic frameworks as well as a tight connection to the actual change in physics were demonstrated. A change in temperature or light induces (physicochemically driven) small volatile apocarotenoid formation leading to conserved retrograde-signaling cascades transducing the environmental read-out. One of the cascades that predated plant terrestrialization is the in this thesis newly discovered putative β-ionone–TF-SUF4–TM- protein–TF-MYB4R1-cascade. But our data show that innovations of these abiotic stress networks in land plants presumably facilitated their conquest. Overall, combining comparative time series experiments with the study of lineage- and species-specific tools including multiple lineages and a total of five species of Phragmoplastophyta shed light on several evolutionary trajectories connecting them and recovered pieces of the plant terrestrialization puzzle.
Keywords: Plant terrestrialization; Apocarotenoids; Carotenoids; Physcomitrium patens; Mesotaenium endlicherianum; Zygnema circumcarinatum; Chara; metabolite profiling; Transcriptomics
