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.
Highlights
The desiccation-tolerant plant Haberlea rhodopensis can withstand months of darkness without any visible senescence
We focus our discussion on processes such as photosynthesis and photorespiration, growth and energy regulation, carbohydrate and lipid metabolism, protein degradation, and autophagy in an attempt to postulate a model for how H. rhodopensis rewires its primary energy metabolism to withstand extreme periods of darkness
As many abiotic stresses, including darkness, and senescence are linked with transient or sustained oxidative stress, we looked at the expression patterns of key antioxidant genes such as SUPEROXIDE DISMUTASE (SOD), CATALASE (CAT), DEHYDROASCORBATE REDUCTASE (DHAR), GLUTATHIONE PEROXIDASE (GPX), GLUTATHIONE-S-TRANSFERASE (GST), and GLUTATHIONE REDUCTASE
Summary
The desiccation-tolerant plant Haberlea rhodopensis can withstand months of darkness without any visible senescence. 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 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. In contrast to other species, the integrity and activity of the photosynthetic apparatus of the desiccation-tolerant H. rhodopensis is preserved months after darkness, and no visible senescence symptoms are observed during this time period (Denev et al, 2012) Such tolerance to long-term darkness is rarely seen in angiosperms, and the molecular mechanisms behind this phenomenon have not been studied. We focus our discussion on processes such as photosynthesis and photorespiration, growth and energy regulation, carbohydrate and lipid metabolism, protein degradation, and autophagy in an attempt to postulate a model for how H. rhodopensis rewires its primary energy metabolism to withstand extreme periods of darkness
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