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Abstract

500 MYA plant terrestrialization fundamentally affected our climate and life on earth. The increased fluctuation and intensity of abiotic factors in terrestrial habitats and the rising oxygen levels created by the first land plants themselves required an elaborate molecular toolkit to mitigate these oxidative stressors. To infer the essential components of this toolkit enabling the conquest of land, we conducted time-resolved stress experiments with the model organism moss Physcomitrium patens and the two genome-sequenced Zygnematophyceaen algae Zygnema circumcarinatum and Mesotaenium endlicherianum – sister to all land plants. We combined transcriptomics, metabolite profiling (chlorophylls, carotenoids (RP-C30-HPLC-UV-Vis) and apocarotenoids (HS-SPME-GC-MS)), photophysiology and morphology to obtain a holistic picture. Carotenoids can be considered as one of the major antioxidants of plant biology and are present in any photosynthetic organism. Thus, utilizing their oxidative breakdown products called apocarotenoids as a stress-intensity read-out likely was highly beneficial for plant terrestrialization. Utilizing state-of-the-art inference models (SWING-RF) our data shows a so far unknown connection of LRR kinase gene expression with the small volatile apocarotenoid β-ionone conserved across the algae-embryophyte divide. Generally, combining a bouquet of methods in a huge time-resolved data set broadens our knowledge about several conserved stress-mitigation hubs of which many were long believed to be land plant-specific.