The seed-to-seedling transition represents a key developmental and metabolic switch in plants. Catabolism of seed storage reserves fuels germination and early seedling emergence until photosynthesis is established. The seed-to-seedling developmental transition is controlled by Polycomb repressive complex 2 (PRC2). However, the coordination of PRC2 activity and its contribution to transcriptional reprogramming during seedling establishment remain unknown. By analyzing H3K27me3 re-distribution and changes in gene transcription in the shoot and root tissues of heterotrophic and photoautotrophic Arabidopsis (Arabidopsis thaliana) seedlings, we reveal two phases of PRC2-mediated gene repression. The first phase is independent of light and photosynthesis and results in the irreversible repression of the embryo maturation program, marked by heterotrophy and reserve storage molecule biosynthesis. The second phase is associated with the repression of metabolic pathways related to germination and early seedling emergence, and H3K27me3 deposition in this phase is sensitive to photosynthesis inhibition. We show that preventing the transcription of the PRC2-repressed glyoxylate cycle gene ISOCITRATE LYASE promotes the vegetative phase transition in PRC2-depleted plants. Our findings underscore a key role of PRC2-mediated transcriptional repression in the coordinated metabolic and developmental switches that occur during seedling emergence and emphasizes the close connection between metabolic and developmental identities.

Plant acclimation occurs through system-wide mechanisms that include proteome shifts, some of which occur at the level of protein synthesis. All proteins are synthesized by ribosomes. Rather than being monolithic, transcript-to-protein translation machines, ribosomes can be selective and cause proteome shifts. In this study, we use apical root meristems of germinating seedlings of the monocotyledonous plant barley as a model to examine changes in protein abundance and synthesis during cold acclimation. We measured metabolic and physiological parameters that allowed us to compare protein synthesis in the cold to optimal rearing temperatures. We demonstrated that the synthesis and assembly of ribosomal proteins are independent processes in root proliferative tissue. We report the synthesis and accumulation of various macromolecular complexes and propose how ribosome compositional shifts may be associated with functional proteome changes that are part of successful cold acclimation. Our study indicates that translation initiation is limiting during cold acclimation while the ribosome population is remodelled. The distribution of the triggered ribosomal protein heterogeneity suggests that altered compositions may confer 60S subunits selective association capabilities towards translation initiation complexes. To what extent selective translation depends on heterogeneous ribo-proteome compositions in barley proliferative root tissue remains a yet unresolved question. This article is part of the discussion meeting issue ‘Ribosome diversity and its impact on protein synthesis, development and disease’.

Background: Specialised anti-herbivory metabolites are abundant in the solanaceous genus Nicotiana. These metabolites include the large family of 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs). Many HGL-DTGs occur exclusively within the Nicotiana genus, but information from the molecular model species N. tabacum, N. benthamiana, and the tree tobacco N. glauca is limited. Objectives: We studied HGL-DTG occurrence and complexity in these species with the aim of providing in-depth reference annotations and comprehensive HGL-DTG inventories. Methods: We analysed polar metabolite extracts in comparison to the previously investigated wild reference species N. attenuata using positive ESI(+) and negative ESI(-) mode electrospray ionisation LC-MS and MS/MS. Results: We provide annotations of 66 HGL-DTGs with in-source and MS/MS fragmentation spectra for selected HGL-DTGs with exemplary fragment interpretations of ESI(+) as well as less studied ESI(-) spectra. We assemble a potential biosynthesis pathway comparing the presence of HGL-DTGs in N. tabacum, N. glauca, and N. benthamiana to N. attenuata. Approximately one-third of HGL-DTGs are chromatographically resolved isomers of hexose, deoxyhexose, or malonate conjugates. The number of isomers is especially high for conjugates with low numbers of deoxyhexose moieties. Conclusions: We extend the number of known HGL-DTGs with a focus on Nicotiana model species and demonstrate that the HGL-DTG family of N. tabacum plants can be surprisingly complex. Our study provides an improved basis with detailed references to previous studies of wild Nicotiana species and enables inference of HGL-DTG pathways with required enzymes for the biosynthesis of this important family of specialised defence metabolites.

Seed-to-seedling transition represents a key developmental and metabolic switch in plants. Catabolism of seed storage reserves fuels germination and early seedling emergence until photosynthesis is established. The developmental transition is controlled by Polycomb repressive complex 2 (PRC2). However, the coordination of PRC2 activity and its contribution to transcriptional reprogramming during seedling establishment is unknown. By analysing the re-distribution of H3K27me3 and changes in gene transcription in shoot and root tissues of heterotrophic and photoautotrophic seedlings, we reveal two phases of PRC2-mediated gene repression. The first phase is independent of light and photosynthesis and results in irreversible repression of the embryo maturation programme, marked by heterotrophy and biosynthesis of reserve storage molecules. The second phase is associated with the repression of metabolic pathways related to germination and early seedling emergence, and H3K27me3 deposition in this phase is sensitive to photosynthesis inhibition. We show that preventing transcription of the PRC2-repressed glyoxylate cycle gene ISOCITRATE LYASE is sufficient to drive the vegetative phase transition in PRC2-depleted plants. This underscores a key role of PRC2 repression in the coordinated metabolic and developmental switches during seedling emergence and emphasizes the close connection between metabolic and developmental identities.