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Establishment of the seedlings is a crucial stage of the plant life cycle. The success of this process is essential for the growth of the mature plant. In Nature, when seeds germinate under the soil, seedlings follow a dark-specific program called skotomorphogenesis, which is characterized by small, non-green cotyledons, long hypocotyl, and an apical hook-protecting meristematic cells. These developmental structures are required for the seedlings to emerge quickly and safely through the soil and gain autotrophy before the complete depletion of seed resources. Due to the lack of photosynthesis during this period, the seed nutrient stocks are the primary energy source for seedling development. The energy is provided by the bioenergetic organelles, mitochondria, and etioplast (plastid in the dark), to the cell in the form of ATP through mitochondrial respiration and etio-respiration processes, respectively. Recent studies suggest that the limitation of the plastidial or mitochondrial gene expression induces a drastic reprogramming of the seedling morphology in the dark. Here, we discuss the dark signaling mechanisms involved during a regular skotomorphogenesis and how the dysfunction of the bioenergetic organelles is perceived by the nucleus leading to developmental changes. We also describe the probable involvement of several plastid retrograde pathways and the interconnection between plastid and mitochondria during seedling development. Understanding the integration mechanisms of organellar signals in the developmental program of seedlings can be utilized in the future for better emergence of crops through the soil. [ABSTRACT FROM AUTHOR]

SUMMARY: When covered by a layer of soil, seedling development follows a dark‐specific program (skotomorphogenesis). In the dark, seedlings consist of small, non‐green cotyledons, a long hypocotyl, and an apical hook to protect meristematic cells. We recently highlighted the role played by mitochondria in the high energy‐consuming reprogramming of Arabidopsis skotomorphogenesis. Here, the role played by plastids, another energy‐supplying organelle, in skotomorphogenesis is investigated. This study was conducted in dark conditions to exclude light signals so as to better focus on those produced by plastids. It was found that limitation of plastid gene expression (PGE) induced an exaggerated apical hook bending. Inhibition of PGE was obtained at the levels of transcription and translation using the antibiotics rifampicin (RIF) and spectinomycin, respectively, as well as plastid RPOTp RNA polymerase mutants. RIF‐treated seedlings also showed expression induction of marker nuclear genes for mitochondrial stress, perturbation of mitochondrial metabolism, increased ROS levels, and an augmented capacity of oxygen consumption by mitochondrial alternative oxidases (AOXs). AOXs act to prevent overreduction of the mitochondrial electron transport chain. Previously, we reported that AOX1A, the main AOX isoform, is a key component in the developmental response to mitochondrial respiration deficiency. In this work, we suggest the involvement of AOX1A in the response to PGE dysfunction and propose the importance of signaling between plastids and mitochondria. Finally, it was found that seedling architecture reprogramming in response to RIF was independent of canonical organelle retrograde pathways and the ethylene signaling pathway. [ABSTRACT FROM AUTHOR]