Deciphering the role of respiration in bioenergetics and metabolism of plants using the model Physcomitrium patens

This thesis delves into the intricate relationship between mitochondrial respiration and plant metabolism, unraveling the pivotal role played by respiration in orchestrating metabolic processes. Over four chapters, it traces the historical progression of research in this field, from the early investigation of cytoplasmic male sterility to the contemporary utilization of genetic manipulation techniques in various plant models. These models have been instrumental in studying the physiological consequences of altering respiratory efficiency, paving the way for a deeper understanding of the interconnectedness of respiration and metabolism. CHAPTER I, the introductory chapter, describes the main components of the respiratory machinery in plants, provides a historical perspective on plant mitochondrial respiration research and sets the stage for understanding the subsequent chapters' experimental findings. It highlights the evolution of experimental techniques and models used to investigate respiratory complexes' roles in metabolic regulation. CHAPTER II presents a newly isolated respiratory mutant in P. patens, cox11, which is completely depleted in Complex IV activity. This mutant was characterized by a different set of experiments, including transcriptomics and metabolomics, that show the metabolic consequences of the depletion of Complex IV in a plant model. The mutants displayed altered growth patterns and strong metabolic disruptions, shedding light on the critical role of respiration in energy mobilization and metabolic homeostasis. CHAPTER III explores the metabolic repercussions of Complex I depletion in the ndufa5 mutant. It uncovers metabolic alterations that are however different from those described for the Complex IV mutant cox11. In this chapter we also study, by exploiting transcrtipomics data, the candidate signaling pathways involved in mitochondrial retrogrdade signaling in P. patens. We propose that the induction of one or more mitochondrial retrograde signaling pathways is at the root of the unique phenotypic characteristics of Complex I-deficient ndufa5 plants. CHAPTER IV investigates subcellular ATP dynamics in response to light in the moss Physcomitrium patens. It underscores the interplay between photosynthesis and mitochondrial respiration in energy provision, even in fully photoautotrophic organisms. We present reporter lines that express a genetically-encoded ATP sensor, both in WT or in Complex I-deficiency backgrounds. This chapter, which is the result of a collaboration with the group of Prof. Markus Scwarzländer, illuminates the dynamic nature of ATP synthesis and highlights the central role of respiration in maintaining metabolic stability. Besides the four main chapters, we also included a series of appendices that are either manuscripts ready for submission or articles that have already been published in peer-reviewed journals. In conclusion, this thesis constitutes a comprehensive investigation into the intricate interplay of mitochondrial respiration and photosynthesis in plant metabolism. By integrating historical context, experimental discoveries, and metabolic insights, it enhances our understanding of how plants adapt to dynamic environmental conditions and optimize their energy utilization.