SNF1-Related Kinase 1 (SnRK1) is an evolutionarily conserved protein kinase with key functions in energy management during stress responses in plants. To address a potential role of SnRK1 under favourable conditions, we performed a metabolomic and transcriptomic characterization of rosettes of 20-d-old Arabidopsis (Arabidopsis thaliana) plants of SnRK1 gain- and loss-of-function mutants during the regular diel cycle. Our results show that SnRK1 manipulation alters the sucrose and trehalose 6-phosphate (Tre6P) relationship, influencing how the sucrose content is translated into Tre6P accumulation and modulating the flux of carbon to the tricarboxylic acid cycle downstream of Tre6P signalling. On the other hand, daily cycles of Tre6P accumulation were accompanied by changes in SnRK1 signaling, leading to a maximum in the expression of SnRK1-induced genes at the end of the night, when Tre6P levels are lowest, and to a minimum at the end of the day, when Tre6P levels peak. The expression of SnRK1-induced genes was strongly reduced by transient Tre6P accumulation in an inducible Tre6P synthase (otsA) line, further suggesting the involvement of Tre6P in the diel oscillations in SnRK1 signaling. Transcriptional profiling of wild-type plants and SnRK1 mutants also uncovered defects that are suggestive of an iron sufficiency response and of a matching induction of sulfur acquisition and assimilation when SnRK1 is depleted. In conclusion, under favourable growth conditions, SnRK1 plays a role in sucrose homeostasis and transcriptome remodelling in autotrophic tissues and its activity is influenced by diel fluctuations in Tre6P levels.
SUCROSE NON-FERMENTING1 (SNF1)-RELATED KINASE 1 (SnRK1) is an evolutionarily conserved protein kinase with key roles in plant stress responses. SnRK1 is activated when energy levels decline during stress, reconfiguring metabolism and gene expression to favour catabolism over anabolism, and ultimately to restore energy balance and homeostasis. The capacity to efficiently redistribute resources is crucial to cope with adverse environmental conditions, and accordingly, genetic manipulations that increase SnRK1 activity are generally associated with enhanced tolerance to stress. In addition to its well-established function in stress responses, an increasing number of studies implicate SnRK1 in the homeostatic control of metabolism during the regular day-night cycle and in different organs and developmental stages. Here, we review how the genetic manipulation of SnRK1 alters central metabolism in several plant species and tissue types. We complement this with studies that provide mechanistic insight into how SnRK1 modulates metabolism, identifying changes in transcripts of metabolic components, altered enzyme activities or direct regulation of enzymes or transcription factors by SnRK1 via phosphorylation. We identify patterns of response that centre on the maintenance of sucrose levels, in an analogous manner to the role described for its mammalian ortholog in the control of blood glucose homeostasis. Finally, we highlight several knowledge gaps and technical limitations that will have to be addressed in future research aiming to fully understand how SnRK1 modulates metabolism at the cellular and whole plant levels.
In plant cells, the conventional route to the vacuole involves the endoplasmic reticulum, the Golgi and the prevacuolar compartment. However, over the years, unconventional sorting to the vacuole, bypassing the Golgi, has been described, which is the case of the Plant-Specific Insert (PSI) of the aspartic proteinase cardosin A. Interestingly, this Golgi-bypass ability is not a characteristic shared by all PSIs, since two related PSIs showed to have different sensitivity to ER-to-Golgi blockage. Given the high sequence similarity between the PSI domains, we sought to depict the differences in terms of post-translational modifications. In fact, one feature that draws our attention is that one is N-glycosylated and the other one is not. Using site-directed mutagenesis to obtain mutated versions of the two PSIs, with and without the glycosylation motif, we observed that altering the glycosylation pattern interferes with the trafficking of the protein as the non-glycosylated PSI-B, unlike its native glycosylated form, is able to bypass ER-to-Golgi blockage and accumulate in the vacuole. This is also true when the PSI domain is analyzed in the context of the full-length cardosin. Regardless of opening exciting research gaps, the results obtained so far need a more comprehensive study of the mechanisms behind this unconventional direct sorting to the vacuole.
Many plants, including Arabidopsis (Arabidopsis thaliana), accumulate starch in the daytime and remobilize it to support maintenance and growth at night. Starch accumulation is increased when carbon is in short supply, for example, in short photoperiods. Mobilization is paced to exhaust starch around dawn, as anticipated by the circadian clock. This diel pattern of turnover is largely robust against loss of day, dawn, dusk, or evening clock components. Here, we investigated diel starch turnover in the triple circadian clock mutant lhy cca1 elf3, which lacks the LATE ELONGATED HYPOCOTYL (LHY) and the CIRCADIAN CLOCK ASSOCIATED1 (CCA1) dawn components and the EARLY FLOWERING3 (ELF3) evening components of the circadian clock. The diel oscillations of transcripts for the remaining clock components and related genes like REVEILLE and PHYTOCHROME INTERACING FACTOR family members exhibited attenuated amplitudes and altered peak time, weakened dawn-dominance, and decreased robustness against changes in the external light-dark cycle. The triple mutant was unable to increase starch accumulation in short photoperiods. However, it was still able to pace starch mobilization to around dawn in different photoperiods and growth irradiances and to around 24 h after the previous dawn in T17 and T28 cycles. The triple mutant was able to slow down starch mobilization after a sudden low-light day or a sudden early dusk, although in the latter case it did not fully compensate for the lengthened night. Overall, there was a slight trend to less linear mobilization of starch. Thus, starch mobilization can be paced rather robustly to dawn despite a major disruption of the transcriptional clock. It is proposed that temporal information can be delivered from clock components or a semi-autonomous oscillator.
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