Molecular Mechanisms Preventing Senescence in Response to Prolonged Darkness in a Desiccation-Tolerant Plant
Creators
- 1. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Institute of Molecular Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Department of Plant Physiology and Molecular Biology, University of Plovdiv, Plovdiv 4000, Bulgaria
- 2. Department Molecular Biology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany
- 3. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Institute of Molecular Biology and Biotechnology, Plovdiv 4000, Bulgaria
- 4. Department Molecular Biology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany ; Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany
- 5. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria
- 6. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Department Willmitzer, Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam, Germany
- 7. Department of Plant and Microbial Biology, University of Zurich, CH-8008 Zurich, Switzerland
- 8. Institute of Fundamental Sciences, Massey University, 4474 Palmerston North, New Zealand
- 9. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Institute of Molecular Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Department of Plant Physiology and Molecular Biology, University of Plovdiv, Plovdiv 4000, Bulgaria
- 10. Department of Life Sciences, Ben Gurion University of the Negev, Beersheva, Israel
- 11. Center of Plant Systems Biology and Biotechnology, Plovdiv 4000, Bulgaria ; Department Molecular Biology, Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam, Germany
Description
Abstract
The desiccation-tolerant plant Haberlea rhodopensis can withstand months of darkness without any visible senescence. Here, we investigated the molecular mechanisms of this adaptation to prolonged (30 d) darkness and subsequent return to light. H. rhodopensis plants remained green and viable throughout the dark treatment. Transcriptomic analysis revealed that darkness regulated several transcription factor (TF) genes. Stress- and autophagy-related TFs such as ERF8, HSFA2b, RD26, TGA1, and WRKY33 were up-regulated, while chloroplast- and flowering-related TFs such as ATH1, COL2, COL4, RL1, and PTAC7 were repressed. PHYTOCHROME INTERACTING FACTOR4, a negative regulator of photomorphogenesis and promoter of senescence, also was down-regulated. In response to darkness, most of the photosynthesis- and photorespiratory-related genes were strongly down-regulated, while genes related to autophagy were up-regulated. This occurred concomitant with the induction of SUCROSE NON-FERMENTING1-RELATED PROTEIN KINASES (SnRK1) signaling pathway genes, which regulate responses to stress-induced starvation and autophagy. Most of the genes associated with chlorophyll catabolism, which are induced by darkness in dark-senescing species, were either unregulated (PHEOPHORBIDE A OXYGENASE, PAO; RED CHLOROPHYLL CATABOLITE REDUCTASE, RCCR) or repressed (STAY GREEN-LIKE, PHEOPHYTINASE, and NON-YELLOW COLORING1). Metabolite profiling revealed increases in the levels of many amino acids in darkness, suggesting increased protein degradation. In darkness, levels of the chloroplastic lipids digalactosyldiacylglycerol, monogalactosyldiacylglycerol, phosphatidylglycerol, and sulfoquinovosyldiacylglycerol decreased, while those of storage triacylglycerols increased, suggesting degradation of chloroplast membrane lipids and their conversion to triacylglycerols for use as energy and carbon sources. Collectively, these data show a coordinated response to darkness, including repression of photosynthetic, photorespiratory, flowering, and chlorophyll catabolic genes, induction of autophagy and SnRK1 pathways, and metabolic reconfigurations that enable survival under prolonged darkness.
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