Survival or starvation: SnRK1 controls rate of resource use in pre-photosynthetic seedlings

In the most perilous part of a green plant’s life cycle, newly germinated seedlings must risk everything to establish photosynthesis and energetic independence. All seeds are stocked with finite nutrient resources in the forms of starch, sugars, storage oils, and storage proteins, but in a small seed like Arabidopsis (Arabidopsis thaliana), these precious resources (∼30 µg) can run out after just 4–5 d (Kircher and Schopfer, 2012). Facing uncertain conditions, seedlings must invest these few resources toward shoot and root growth in a strategic and timely fashion in order to optimize their chance of survival. It follows that multiple regulatory mechanisms have evolved to coordinate environmental and cellular cues with the mobilization of carbon, nitrogen, and energy reserves in seedlings. Throughout eukaryotes, many aspects of cellular energy status are signaled via a group of conserved regulatory kinases, which in plants are called Sucrose nonfermenting-Related protein Kinases (SnRKs). Activation of SnRK1 activity in several plant tissues signals imminent stress and carbon starvation, leading to massive transcriptional and post-translational changes that suppress growth and conserve energy (Baena-Gonzalez and Sheen, 2008). The period between germination and seedling establishment involves rapid changes in metabolism and energy status, and the likely prospect of starvation. In their recent Plant Cell paper, Markus Henninger et al. combined genetic, transcriptomic, and metabolomic approaches to elucidate a role for the master energy regulator SnRK1 at this crucial phase of plant metabolism. To assess SnRK1 function in developing seedlings, the authors established an effective inducible loss-of-function method targeting the catalytic subunits of SnRK1: SnRK1α1 and SnRK1α2. In snrk1α1/α2 seedlings, growth ceased 3 d after germination, and chlorophyll content and chlorophyll fluorescence only accumulated transiently thereafter. These observations indicated that SnRK1 activity is essential for effective seedling establishment. The establishment phenotype of snrk1α1/α2 was largely rescued by addition of easily metabolizable carbohydrates like glucose to the growth medium. Furthermore, the transcriptional differences between wild-type and snrk1α1/α2 seedlings, which were substantial under control conditions, were greatly diminished by the presence of glucose. This sugar-rescue seedling phenotype is characteristic of mutants deficient in the metabolism of storage compounds to glucose (gluconeogenesis), which is a necessary metabolic process prior to establishment of photosynthesis. Sure enough, when the author’s detailed resource mobilization in seedlings post-germination, loss of Snrk1α1/α2 led to lower rates of storage lipid and storage protein drawdown and consequently lower levels of metabolically available sugars and amino acids (Figure). Reduced sugar and amino acid availability in germinated snrk1α1/α2 seedlings. Sugar content (A) or free amino acid content (B) were measured in wild type (col-0) and snrk1α1/α2 seedlings post-germination in the dark, with or without transfer to light after 3 days. Adapted from Henninger et al. (2021), Figure 4. Reduced sugar and amino acid availability in germinated snrk1α1/α2 seedlings. Sugar content (A) or free amino acid content (B) were measured in wild type (col-0) and snrk1α1/α2 seedlings post-germination in the dark, with or without transfer to light after 3 days. Adapted from Henninger et al. (2021), Figure 4. The mechanisms behind Snrk1α1/α2 control of reserve mobilization were pursued through a post-germination RNA-seq time course. In line with metabolite level analysis, snrk1α1/α2 seedlings displayed reduced expression of transcripts for certain enzymes in lipid β-oxidation and amino acid catabolism, along with the key initial enzymes of gluconeogenesis: phosphoenolpyruvate carboxykinase and cytosolic pyruvate, phosphate dikinase (cyPPDK). The transcriptional profile of snrk1α1/α2 seedlings was similar to that of known targets of the transcription factor bZIP63 (Pedrotti et al., 2018), which itself is a subject to SnRK1 regulatory phosphorylation. Promoter reporter assays in leaf protoplasts revealed that exogenous bZIP63 expression increased ProcyPPDK activation but only in the presence of co-expressed SnRK1. Subsequent multi-pronged cyPPDK promoter analyses discovered that bZIP63 bound to specific locations on the PPDK gene. These results illustrate a clear SnRKα1/α2 regulatory mechanism in seedlings, where phosphorylation and activation of the bZIP63 lead to enhanced expression of the key gluconeogenic enzyme PPDK. Taken together, the results of this study indicate that SnRK1 plays a major role in orchestrating seed resource mobilization. Whether this role for SnRK1 differs between oilseeds (as described here) and other types of plant seeds will be an important area of future research.

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