Molecular Mechanisms Preventing Senescence in Response to Prolonged Darkness in a Desiccation-Tolerant Plant

Abstract

The desiccation-tolerant plant 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. 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 ,, ,, and were up-regulated, while chloroplast- and flowering-related TFs such as, ,, , and were repressed. , 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 () or repressed (, , and). 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.

A Biostimulant Obtained from the Seaweed Ascophyllum nodosum Protects Arabidopsis thaliana from Severe Oxidative Stress

“…A knockout mutant of a gene coding oleosin-B3-like protein is hypersensitive to salt stress [87]. Lipid reconfigurations occur during oxidative stress balancing energy metabolism and mitigating the oxidative damage [23,88].…”

“…Electrolyte leakage measurements were performed at the rosette stage by checking conductivity with a HI 8733 conductivity meter (Hanna Instruments, Woonsocket, RI, USA) as described in Reference [23]. Visualization of dead cells was done using detached rosette leaves employing a slightly modified version of trypan blue staining protocol explained in Reference [105].…”

“…Lipids were extracted from 50 (±5) mg ground freeze-dried leaf material using the methyl tert-butyl ether (MTBE) method [119]; data were analyzed as reported [23]. Raw lipid intensities were log 2 transformed to bring them closer to normal distribution and to exclude the dominant effect of extreme small/large values [120].…”

“…Both molecular priming and acclimation alter transcriptomes and metabolomes, resulting in molecular re-adjustments that are necessary and sufficient to provide stress protection [21]. Although not deeply studied yet, a re-adjustment of the lipidome is an important part of the metabolome that captures the entirety of lipids in a biological system [22,23].…”

Autophagy in Plants: Both a Puppet and a Puppet Master of Sugars

“…Tre was suggested to induce autophagy (Williams et al, 2015), with possible involvement of SnRK1 (Asami et al, 2018). Interestingly, non-Tre accumulating resurrection species such as Haberlea rhodopensis stays green in prolonged darkness for several months, and SnRK1 seems to be a key player (Durgud et al, 2018).…”