Cell growth and homeostasis are disrupted in Arabidopsis rns2-2 mutants

The salvage pathway that recycles rRNA is shown to be important in maintaining normal nucleoside levels and cellular homeostasis in plants.
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Turnover of ribosomal RNA is essential to maintain cellular homeostasis. Arabidopsis thaliana plants missing the ribonuclease RNS2 are deficient in this process and have constitutive autophagy. Using transcriptome and metabolite analyses, Morriss et al. found that defects in rRNA recycling cause changes in carbon flux through the pentose phosphate pathway in order to produce metabolites needed to synthesize nucleosides.

Model of the effect of the rns2-2 mutation on arabidopsis metabolism.
Model of the effect of the rns2-2 mutation on arabidopsis metabolism. Integration of transcriptome and metabolome data suggests that carbon flux is shuttled through the PPP. Since rns2-2 plants are deficient in rRNA turnover and nucleotide salvage, the increased carbon flux through the PPP pathway may be needed to generate ribose-5-phosphate for de novosynthesis of nucleotides to maintain cellular homeostasis. Changes in metabolism also result in increased NADPH levels. This increase causes accumulation of reactive oxygen species (ROS) that in turn signal the activation of the autophagy machinery. Green boxes indicate enzymes encoded by a gene downregulated in rns2-2, and red boxes upregulated. Green and red arrows indicate metabolites with lower and higher levels in rns2-2, respectively. F6P, fructose-6-phosphate; G6P, glucose-6-phosphate; 6PGL, 6-phosphogluconolactone; 6PG, 6-phosphogluconate; Ru5P, ribulose-5-phosphate; Xu5P, xylulose-5-phosphate; GAP, glyceraldehyde-3-phosphate; E4P, erythrose-4-phosphate; R5P, ribose-5-phosphate; S7P, sedoheptulose-7-phosphate; RuBP, ribulose-1,5-bisphosphate; 3PG, 3-phosphoglycerate; BPG, 1,3-bisphosphoglycerate; DHAP, dihydroxyacetone-phosphate; SBP, sedoheptulose-1,7-bisphosphate; FBP, fructose-1,6-bisphosphate; pgi, glucose phosphate isomerase; g6pdh, glucose-6-phosphate dehydrogenase; pgl, 6-phosphogluconolactonase; rpe, ribulose-5-phosphate epimerase; tal, transaldolase; tkl, transketolase; fbpase, fructose-2,6-bisphosphatase; fba, fructose-bisphosphate aldolase; rpi, ribose-5-phosphate isomerase; sbpase, sedoheptulose-1,7-bisphosphatase; tpi, triosephosphate isomerase; gap, glyceraldehyde-3-phosphate dehydrogenase; pgk, phosphoglycerate kinase; rbc, ribulose-1,5-bisphosphate carboxylase/oxygenase; prk, phosphoribulokinase.

Metabolic changes also increase reactive oxygen species that signal the activation of autophagy, likely to compensate for the lack of rRNA degradation. Lack of rRNA recycling in rns2-2 cells triggers a change in carbon flux, which is redirected through the PPP to produce ribose-5-phosphate for de novo nucleoside synthesis. rRNA or ribosome turnover is thus essential for cellular homeostasis, probably through maintenance of nucleoside levels as part of the salvage pathway.

Reference

Morriss, S. C., Liu, X., Floyd, B. E., Bassham, D. C., & MacIntosh, G. C. (2017). Cell growth and homeostasis are disrupted in arabidopsis rns2-2 mutants missing the main vacuolar RNase activity. Annals of Botany, 120(6), 911–922. https://doi.org/10.1093/aob/mcx099


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