Action of gibberellins on growth and metabolism of Arabidopsis plants associated with high concentration of carbon dioxide

Abstract

Although the positive effect of elevated CO(2) concentration [CO(2)] on plant growth is well known, it remains unclear whether global climate change will positively or negatively affect crop yields. In particular, relatively little is known about the role of hormone pathways in controlling the growth responses to elevated [CO(2)]. Here, we studied the impact of elevated [CO(2)] on plant biomass and metabolism in Arabidopsis (Arabidopsis thaliana) in relation to the availability of gibberellins (GAs). Inhibition of growth by the GA biosynthesis inhibitor paclobutrazol (PAC) at ambient [CO(2)] (350 µmol CO(2) mol(-1)) was reverted by elevated [CO(2)] (750 µmol CO(2) mol(-1)). Thus, we investigated the metabolic adjustment and modulation of gene expression in response to changes in growth of plants imposed by varying the GA regime in ambient and elevated [CO(2)]. In the presence of PAC (low-GA regime), the activities of enzymes involved in photosynthesis and inorganic nitrogen assimilation were markedly increased at elevated [CO(2)], whereas the activities of enzymes of organic acid metabolism were decreased. Under ambient [CO(2)], nitrate, amino acids, and protein accumulated upon PAC treatment; however, this was not the case when plants were grown at elevated [CO(2)]. These results suggest that only under ambient [CO(2)] is GA required for the integration of carbohydrate and nitrogen metabolism underlying optimal biomass determination. Our results have implications concerning the action of the Green Revolution genes in future environmental conditions.

Figure 1.

Phenotypic changes of Arabidopsis plants caused by treatment with PAC and/or GA grown at ambient or elevated [CO₂]. A, Phenotypes of 28-d-old plants grown at 350 or 750 µmol CO₂ mol⁻¹. Note the reversion to normal growth of PAC-treated plants at elevated [CO₂]. B, Rosette fresh weight. C, Rosette dry weight. D, Rosette area. E, Number of rosette leaves. F, Relative growth rate. G, Relative rosette area expansion rate. H, Specific leaf area. I, Root fresh weight. J, Shoot-to-root ratio. Asterisks indicate values determined by Student’s t test to be significantly different from control plants at the shown [CO₂] (P < 0.05). Values are means ± se of four independent experiments. DW, Dry weight; FW, fresh weight.

Figure 2.

Levels of sugars, starch, malate, and fumarate in plants treated with PAC and/or GA. Carbohydrates and organic acids were measured in rosettes at the end of the light period (white sectors) and the end of dark period (gray sectors) in material harvested from plants grown at 350 or 750 µmol CO₂ mol⁻¹. A, Fru. B, Glc. C, Suc. D, Starch. E, Malate. F, Fumarate. G, Rate of starch accumulation. H, Rate of accumulation of sugars (sum of Suc, Glc, and Fru). I, Rate of malate accumulation. J, Rate of fumarate accumulation. Accumulation rates were calculated from the net difference in metabolite contents at the end of the night and the end of the day. Asterisks indicate values determined by Student’s t test to be significantly different from control plants at the shown [CO₂] (P < 0.05). Values are means ± se of four independent experiments. FW, Fresh weight.

Figure 3.

Levels of chlorophyll, nitrate, total amino acids, protein, and NR activity in plants treated with PAC and/or GA. A, Chlorophyll. B, Nitrate. C, Total amino acids. D, Protein. E, NR activity. F, NR activation state. Measurements were done using rosettes harvested at the end of the light period from plants grown at 350 or 750 µmol CO₂ mol⁻¹. Asterisks indicate values determined by Student’s t test to be significantly different from the control plants at the shown [CO₂] (P < 0.05). Values are means ± se of four independent experiments. FW, Fresh weight.

Figure 4.

Enzyme activities in shoots of plants treated with PAC and/or GA. A, Initial Rubisco activity. B, Total Rubisco activity. C, Rubisco activation. D, PGK. E, TK. F, Aldolase. G, GAPDH (NADP). H, AGPase. I, MDH (NAD). J, Initial MDH (NADP) activity. K, Total MDH (NADP) activity. L, MDH (NADP) activation. Measurements were done using Arabidopsis rosettes at the end of the light period from plants grown at 350 or 750 µmol CO₂ mol⁻¹. Asterisks indicate values determined by Student’s t test to be significantly different from the control plants at the shown [CO₂] (P < 0.05). Values are means ± se of four independent experiments. FW, Fresh weight.

Figure 5.

Pyridine nucleotide levels in shoots of Arabidopsis plants treated with PAC and/or GA. A, NAD. B, NADH. C, NADP. D, NADPH. E, NAD/NADH ratio. F, NADP/NADPH ratio. Levels were measured in rosettes at the end of the light period in material harvested from plants grown at 350 or 750 µmol CO₂ mol⁻¹. Asterisks indicate values determined by Student’s t test to be significantly different from the control plants at the shown [CO₂] (P < 0.05). Values are means ± se of four independent experiments. FW, Fresh weight.