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Decoding the environmental adaptation of plant stem cell control

Final Report Summary - STEMCELLADAPT (Decoding the environmental adaptation of plant stem cell control)

As sessile organisms, plants are exposed to extreme variations in environmental conditions over the course of their lives. Since plants grow and initiate new organs continuously, they have to modulate the underlying developmental program accordingly to cope with this challenge. At the heart of this extraordinary developmental plasticity are pluripotent stem cells, which are maintained during the entire life-cycle of the plant and that are embedded within dynamic stem cell niches. Consequently, stem cell systems in plants respond strongly to variations in environmental conditions, in order to synchronize stem cell behavior with the overall growth status of the plant. While the complex regulatory principles of plant stem cell control under artificial constant growth conditions begin to emerge, virtually nothing is known about how this circuit adapts to variations in the environment. In our project we study cell behavior in the apical stem cell niche and define the epigenetic and transcriptional states of stem cells and niche cells to elucidate how these cells are reprogrammed by environmental influences using advanced live imaging and cell type specific genomics, respectively. To elucidate how environmental stimuli are sensed by the stem cell regulatory system, we systematically tested known regulators of light, temperature and metabolic signaling for their role in stem cell activation after germination, both by traditional, as well as by advanced cell-type specific genetics. We have identified wave-length specific upstream regulators and components in the downstream processing pathway that integrate light and nutrient signaling. Surprisingly, we identified the evolutionary conserved TOR kinase as the central regulator of stem cell activation in plants, which also plays an important role in coupling metabolism and development in animals, including humans. Furthermore, we have successfully developed a 3D imaging and analysis workflow, which allows us to quantitatively record a large number of important parameters of the apical stem cell system under divergent environments. Our results include the identification of tissue layer specific cellular responses to changing light and temperature stimuli, as well as compensatory changes in the proliferative behavior of cells, which reflect the behaviour found in genetic variants found in diverse habitats. Last, but not least, we have established advanced technologies to carry out genome wide chromatin profiling on small cell populations, such as stem cells and are currently applying them to create a genomic baseline of the epigenetic state of stem cells and niche cells. Together, our work funded through the ERC program has given an unprecedented insight into how plant stem cells perceive environmental signals and how their transcriptional and epigenetic programs respond under changing environments. In addition, our experiments have revealed that the mechanisms of short-term environmental acclimatization of the regulatory system converge with the long-term evolutionary adaptation of organisms to their environment.