Potassium Application Boosts Photosynthesis and Sorbitol Biosynthesis and Accelerates Cold Acclimation of Common Plantain ( Plantago major L.)

Abstract

Potassium (K) is essential for the processes critical for plant performance, including photosynthesis, carbon assimilation, and response to stress. K also influences translocation of sugars in the phloem and regulates sucrose metabolism. Several plant species synthesize polyols and transport these sugar alcohols from source to sink tissues. Limited knowledge exists about the involvement of K in the above processes in polyol-translocating plants. We, therefore, studied K effects in Plantago major, a species that accumulates the polyol sorbitol to high concentrations. We grew P. major plants on soil substrate adjusted to low-, medium-, or high-potassium conditions. We found that biomass, seed yield, and leaf tissue K contents increased in a soil K-dependent manner. K gradually increased the photosynthetic efficiency and decreased the non-photochemical quenching. Concomitantly, sorbitol levels and sorbitol to sucrose ratio in leaves and phloem sap increased in a K-dependent manner. K supply also fostered plant cold acclimation. High soil K levels mitigated loss of water from leaves in the cold and supported cold-dependent sugar and sorbitol accumulation. We hypothesize that with increased K nutrition, P. major preferentially channels photosynthesis-derived electrons into sorbitol biosynthesis and that this increased sorbitol is supportive for sink development and as a protective solute, during abiotic stress.

Keywords: Plantago; cold stress; phloem; photosynthesis; potassium; sorbitol; sucrose.

Figure 1

Effect of different soil K levels on biomass of P. major. (A) Exemplary pictures of 5-week old P. major plants grown under 3 different doses of soil K. (B) Development of leaf number over a time of 15 days (data represent means from n = 15 plants per data point ± SD). (C) Shoot fresh weight; (D) shoot dry weight; (E) shoot water content; (F) inflorescence height; (G) number of seeds per inflorescence, and (H) root dry weights of K1 to K3-grown plants (bars represent means from n = 6 roots per K condition ± SE). (C–G) Boxplots based on values from at least n = 12 plants per soil K level. Center lines within boxes represent median, crosses are the mean values. The notches are defined as +/− 1.58 × IQR/sqrt (n) and represent the 95% confidence interval for each median. Different letters denote significant changes between K treatments, according to one-way ANOVA with post-hoc Tukey HSD test (p = 0.05).

Figure 2

Effect of different soil K levels on nutrient concentrations in shoots of P. major plants. (A) Potassium content, (B) sodium content, (C) ammonium content, (D) magnesium content, (E) calcium content, (F) nitrate content, (G) phosphate content, (H) sulfate content, and (I) chloride content. Boxplots show distribution of n = 7 replicates. Center lines show the medians; box limits indicate the 25th and 75th percentiles. Different letters above boxes indicate significant differences between the K conditions, according to one-way ANOVA with post-hoc Tukey HSD test (p = 0.05).

Figure 3

Effect of different soil K levels on photosynthetic parameters and photosynthetic pigments. (A) Electron transfer rate (ETR) describing how many electrons were generated from the collected photons at photosystem II, depending on the light intensity. (B) Quantum yield of photosynthesis [Y(II)], depending on the light intensity. (C) Non-photochemical quenching [Y(NPQ)], depending on the light intensity. (D) Non-regulated quenching [Y(NO)], depending on the light intensity. (E) Chlorophyll A and B contents of leaves. (F) Summarized content of violaxanthin (Vx), antheraxanthin (Ax), and zeaxanthin (Zx). (G) Zeaxanthin synthesis (= Zx/(Vx + Ax + Zx) × 100%) after transfer of leaves from dark to high light (750 µE). Four plants were analyzed per condition. Data points are means ± SE. Light curves were recorded using continuous light, incrementally increasing data in (F–G) are means from n = 5 replicates ± SE. Different letters above bars indicate significant differences, according to one-way ANOVA with post-hoc Tukey HSD test (p < 0.05).

Figure 4

Effect of different soil K levels on the gas exchange parameters and the assimilation rate of P. major plants. (A) CO₂ assimilation rate recorded in the light (A), (B) stomatal conductance (g) in the light, (C–F) assimilate contents of shoots—(C) sorbitol, (D) sucrose, (E) glucose, and (F) starch. Bars are means of n = 4 (A–D) or n = 5 (D–F) biological replicates ± SE. Different letters above bars indicate significant differences according to one-way ANOVA, with post-hoc Tukey HSD test (p < 0.05).

Figure 5

Effect of different soil K levels on phloem exudates. (A) K⁺ level; (B) Ca²⁺ level; (C) sum of sorbitol and sucrose; (D) sorbitol to sucrose ratio, and (E) sugar profile in phloem. Boxplots are based on values from n = 15 plants per soil K level. Center lines within boxes represent median, and crosses are mean values. The notches are defined as +/− 1.58 × IQR/sqrt (n) and represent the 95% confidence interval for each median. Bars are means from n = 15 replicates ± SD. Different letters indicate significant differences between K conditions, according to the one-way ANOVA with post-hoc Tukey HSD test (p < 0.05).

Figure 6

Effect of cold stress on plant growth and sugar accumulation in P. major plants grown on three different soil K levels. (A) Representative phenotypes of plants, two days after transferring from 20 °C to 4 °C. (B) Water content of shoots of plants before (0 days) and after transferring to cold condition. (C) Shoot glucose concentration; (D) shoot fructose concentration; (E) shoot sucrose concentration; (F) shoot sorbitol concentration; (G) shoot maltose concentration; and (H) shoot starch concentration during cold stress. Values are means from n = 5 plants ± SE. Different letters above bars denote significant differences according to one-way ANOVA with post-hoc Tukey HSD test (p < 0.05).

Figure 7

Effect of cold stress on the expression of sorbitol and sucrose-related genes. (A) Relative SDH mRNA levels, (B) relative SUC2 mRNA levels, (C) relative PMT1 mRNA levels, and (D) relative PMT2 mRNA levels. Bars show means from n = 6 biological replicates ± SE. Different letters above bars denote significant differences between means, according to one-way ANOVA, with post-hoc Tukey HSD testing (p > 0.05).