Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase‐1 mutant gin2‐1 to high light

Abstract

Summary Stress responses in plants imply spatio‐temporal changes in enzymes and metabolites, including subcellular compartment‐specific re‐allocation processes triggered by sudden changes in environmental parameters. To investigate interactions of primary metabolism with abiotic stress, the gin2‐1 mutant, defective in the sugar sensor hexokinase 1 (HXK1) was compared with its wildtype Landsberg erecta (Ler) based on time resolved, compartment‐specific metabolome and proteome data obtained over a full diurnal cycle. The high light sensitive gin2‐1 mutant was substantially delayed in subcellular re‐distribution of metabolites upon stress, and this correlated with a massive reduction in proteins belonging to the ATP producing electron transport chain under high light, while fewer changes occurred in the cold. In the wildtype, compounds specifically protecting individual compartments could be identified, e.g., maltose and raffinose in plastids, myo‐inositol in mitochondria, but gin2‐1 failed to recruit these substances to the respective compartments, or responded only slowly to high irradiance. No such delay was obtained in the cold. At the whole cell level, concentrations of the amino acids, glycine and serine, provided strong evidence for an important role of the photorespiratory pathway during stress exposure, and different subcellular allocation of serine may contribute to the slow growth of the gin2‐1 mutant under high irradiance.

Differential Contribution of P5CS Isoforms to Stress Tolerance in Arabidopsis

“…However, partitioning studies indicated that the predominant accumulation of proline in the cytosol and in chloroplasts of osmotically stressed potato leaves and in salt-stressed sugar beet may account for a relevant osmotic function of proline in these compartments (Büssis and Heineke, 1998;Hossain et al, 2017). Compartment-specific metabolite analyses in cold-stressed or high-light-exposed Arabidopsis rosettes confirmed that the distribution of proline within the cells changes in response to stress and is additionally dependent on changes in carbon metabolism (Fürtauer et al, 2016;Hörmiller et al, 2017;Küstner et al, 2019). Genetically encoded nanosensors for in vivo analysis of proline concentrations and osmotic potential, as they are already available for other amino acids and the subcellular redox potential, will need to be developed and used to determine the precise contribution of proline to osmotic adjustment (Bogner and Ludewig, 2007;Schwarzländer et al, 2016;Sanford and Palmer, 2017).…”

Indications for a Central Role of Hexokinase Activity in Natural Variation of Heat Acclimation in Arabidopsis thaliana

“…Enzymatic reactions catalyzed by SPS, GlcK and FrcK, and invertases constitute a futile cycle of sucrose biosynthesis and degradation which has previously been discussed in context of metabolic stabilization under environmental changes, e.g., low temperature [ 29 , 30 , 31 ]. In context of recent findings, which provided evidence for central metabolic role of hexokinase 1 in response to high light stress [ 32 ], it remains tempting to speculate that differential GlcK and FrcK activities in Ct-1 and Rsch-4 explain different subcellular sucrose cycling capacities resulting in different stress acclimation capacities. However, in the present study no significant difference was detected between NPS rates of Ct-1 and Rsch-4, which suggests similar capacities of both accessions to photosynthetically acclimate to H and HHL.…”

Roles of Organellar RNA-Binding Proteins in Plant Growth, Development, and Abiotic Stress Responses

“…Beyond organelles, it will be of great interest to investigate how nCMRBP-mediated organellar retrograde signaling (ORS) influences the reprogramming of the expression of stress-responsive nuclear genes, and the organellar and nuclear epigenetic modifications for stress priming and memory [ 101 , 118 , 119 , 120 , 121 ]. Although the study of organellar proteomics and metabolomics is far behind than those in the nucleus and cytoplasm, recent studies emphasize the importance of homeostasis between the nucleus and organelles in plant acclimation to environmental changes [ 122 , 123 , 124 , 125 ]. With these omics data, future tasks are to identify novel ORS molecules and pathways, which will widely expand our understanding of crosstalk between the nucleus and organelles.…”