Oligosaccharide production and signaling correlate with delayed flowering in an Arabidopsis genotype grown and selected in high [CO2]

Abstract

Since industrialization began, atmospheric CO2 ([CO2]) has increased from 270 to 415 ppm and is projected to reach 800-1000 ppm this century. Some Arabidopsis thaliana (Arabidopsis) genotypes delayed flowering in elevated [CO2] relative to current [CO2], while others showed no change or accelerations. To predict genotype-specific flowering behaviors, we must understand the mechanisms driving flowering response to rising [CO2]. [CO2] changes alter photosynthesis and carbohydrates in plants. Plants sense carbohydrate levels, and exogenous carbohydrate application influences flowering time and flowering transcript levels. We asked how organismal changes in carbohydrates and transcription correlate with changes in flowering time under elevated [CO2]. We used a genotype (SG) of Arabidopsis that was selected for high fitness at elevated [CO2] (700 ppm). SG delays flowering under elevated [CO2] (700 ppm) relative to current [CO2] (400 ppm). We compared SG to a closely related control genotype (CG) that shows no [CO2]-induced flowering change. We compared metabolomic and transcriptomic profiles in these genotypes at current and elevated [CO2] to assess correlations with flowering in these conditions. While both genotypes altered carbohydrates in response to elevated [CO2], SG had higher levels of sucrose than CG and showed a stronger increase in glucose and fructose in elevated [CO2]. Both genotypes demonstrated transcriptional changes, with CG increasing genes related to fructose 1,6-bisphosphate breakdown, amino acid synthesis, and secondary metabolites; and SG decreasing genes related to starch and sugar metabolism, but increasing genes involved in oligosaccharide production and sugar modifications. Genes associated with flowering regulation within the photoperiod, vernalization, and meristem identity pathways were altered in these genotypes. Elevated [CO2] may alter carbohydrates to influence transcription in both genotypes and delayed flowering in SG. Changes in the oligosaccharide pool may contribute to delayed flowering in SG. This work extends the literature exploring genotypic-specific flowering responses to elevated [CO2].

Fig 1. Experimental set up and harvest stage.

(a) The Control and Selected Genotypes (CG and SG) were grown both at ‘current’ atmospheric [CO₂] (380 ppm) and projected future [CO₂] (700 ppm). Plants were harvested just prior to visible emergence of the reproductive stem (= bolt) for CG at 380 and 700 ppm, and for SG at 380 ppm using visible bolting of plants that were planted one-week prior as a cue to harvest. For SG at 700 ppm, plants were harvested at the analogous leaf number to SG grown at 380 ppm. Blue and grey bars represent time. Images are not originals but used for illustrative purposes only and leaf numbers are approximate. Bolt heights are exaggerated for visibility. Illustrations drawn by Hannah Kinmonth-Schultz using InkSkape and used with permission under a CC BY 4.0 license. (b) Average leaf number at harvest across replicates is shown for reference. Error bars are standard deviation. Although not included in this analysis, the leaf number of SG just prior to flowering at 700 ppm is shown for comparison.

Fig 2. Transcript count differed between the Control and Selected Genotypes (CG and SG) and within genotypes across 380 and 700 ppm [CO₂].

(a-f) Each grey line (background) represents the mean relativized count (centered log ratio) of the 16,472 unique transcript identifiers in this dataset. Colored lines in bold represent those transcript identifiers with effect sizes greater than ± 1 in each comparison, while the lighter sections in each plot allow visualization of how those same transcripts respond across genotypes or within the other genotype. (a-b) Transcript identifiers showing an increase (a) and decrease (b) from CG to SG. (c-d, bold lines) Transcript identifiers showing an increase (c) and decrease (d) in CG from 380 to 700 ppm [CO₂]. For reference, the same transcripts are visible in SG (light lines). (e-f, bold lines) Transcript identifiers showing an increase (e) and decrease (f) in SG from 380 to 700 ppm [CO₂]. For reference, the same transcripts are visible in CG (light lines). Green lines in d-f show flowering genes found to have effect sizes greater than ± 1.