Steady-state and dynamic photosynthetic characteristics of shade-tolerant species Panax notoginseng in response to nitrogen levels

doi:10.17521/cjpe.2021.0452

Abstract

Abstract:

Aims Nitrogen (N) is essential for the photosynthesis of plants. Shade plants are mostly exposed to dynamic light under natural growth conditions. However, little is known about the role of N levels in the photosynthetic regulation of shade plants under dynamic light. The objective of present study was to elucidate the mechanisms involved in the effect of N on dynamic photosynthesis in the typically shade-tolerant species Panax notoginseng.

Methods The gas exchange parameters and the activity and amount of Calvin cycle enzyme/proteins were examined under dynamic and steady light conditions in P. notoginseng grown under low N (LN, 112.5 kg·hm^-2) and high N (HN, 450.0 kg·hm^-2), respectively.

Important findings N content per unit of leaf area (N_area) was negatively correlated with the induction state at 60s of light (IS₆₀) and positively correlated with the time required to reach 90% of photosynthetic steady state (t_P90) and 100% of photosynthetic steady state (t_P-steady), suggesting that N_area does not regulate the photosynthetic induction during dynamic light by the total activity of ribulose-1,5-bisphosphate carboxylase (Rubisco). Moreover, a short low light interval only slightly decreased the activity of Rubisco, but significantly reduced the activity of fructose-1,6-bisphosphatase (FBPase) and sedoheptulose-1,7-bisphosphatase (SBPase); when the sunfleck of high intensity appeared suddenly, Rubisco was still highly active, but SBPase and FBPase need to be reactivated to match Rubisco activity, so that photosynthetic induction after low light intervals is largely limited by reactivation of SBPase and FBPase. Furthermore, the content of Rubisco was higher than that of FBPase and SBPase. During the high light period of dynamic light, HN leaves need to activate a higher proportion of FBPase and SBPase and a longer period of time to resume photosynthesis. The results of present study reveal that under dynamic light condition, LN could alleviate the decline of photosynthetic induction rate, while HN exacerbated the decline of photosynthetic induction rate. The limitation in enzymes related to the ribulose-1,5-disphosphate (RuBP) may be one of the reasons why HN exacerbates the decline of photosynthetic induction rate under dynamic light condition.

Key words: shade-tolerant species, dynamic light, photoinduction, low nitrogen, high nitrogen, Panax notoginseng

ZHANG Jin-Yan, CUN Zhu, SHUANG Sheng-Pu, HONG Jie, MENG Zhen-Gui, CHEN Jun-Wen. Steady-state and dynamic photosynthetic characteristics of shade-tolerant species Panax notoginseng in response to nitrogen levels[J]. Chin J Plant Ecol, 2023, 47(3): 331-347.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0452

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Figures/Tables 9

Fig. 1 Leaf nitrogen (N) content, chlorophyll (Chl) concentration and specific leaf area (SLA) of Panax notoginseng at different N levels. HN, high nitrogen; LN, low nitrogen. * indicates significant differences between the two N treatments (p < 0.05).

Fig. 2 Net photosynthetic rate (Pn), stomatal conductance (gs), intercellular CO2 concentration (Ci) and transpiration rate (Tr) of Panax notoginseng in response to photosynthetic photon flux density (PPFD) at two different nitrogen levels (mean ± SD). HN, high nitrogen; LN, low nitrogen. * indicates significant differences between the two nitrogen treatments (p < 0.05).

Fig. 3 Gas exchange parameters of leaves of Panax notoginseng under irregular dynamic light condition (mean ± SD). A, B, Net photosynthetic rates (Pn) under low nitrogen (LN) and high nitrogen (HN) conditions. The bars at the top of the figures show the net photosynthetic rates under high light (HL, 800 μmol·m-2·s-1, white) and low light (LL, 50 μmol·m-2·s-1, grey) conditions. The leaves were exposed to high light for 20-40 min until the net photosynthetic rates stabilized. After that, the leaves were exposed to changing light conditions. The grey bars from left to right represent low light at 60, 120, 300 and 600 s. The white bars from left to right represent high light at 300, 300, 600 and 900 s. C, Induction state of net photosynthetic rates (IS) after low light intervals of different durations. D-G, Integrated net photosynthetic rates during high light period after 60, 120, 300 and 600 s low light intervals. * indicates significant differences between the two nitrogen treatments (p < 0.05).

Fig. 4 Intercellular CO2 concentration (Ci), stomatal conductance (gs) and transpiration rate (Tr) under two dynamic light conditions, and photosystem II photoinhibition induced by dynamic light of Panax notoginseng (mean ± SD). The bars at the top of A?F show the high light (800 μmol·m?2·s?1, white) and low light (50 μmol·m?2·s?1, grey) periods. Fv/Fm, maximum photochemistry efficiency of photosystem II; HN, high nitrogen; LN, low nitrogen. Different lowercase letters in G indicate significant differences (p < 0.05).

Fig. 5 Gas exchange parameters of Panax notoginseng under regular dynamic light condition (mean ± SD). In A and B, after photosynthetic rate was stabilized, the light intensity alternated between high light (HL, 800 μmol·m-2·s-1, white) and low light (LL, 50 μmol·m-2·s-1, grey) every 60 s under fluctuating light. In C, net photosynthetic rate (Pn) under steady-state high light was 100%, net photosynthetic rate under fluctuating light was the percentage of net photosynthetic rate under steady-state high light. Pnmax, maximum net photosynthetic rate. HN, high nitrogen; LN, low nitrogen. * indicates significant differences between the two nitrogen treatments (p < 0.05).

Fig. 6 Correlation between gas exchange parameters of Panax notoginseng. IS60, induction state at 60 s of light; Narea, nitrogen content per unit leaf area; Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase; tP90, time required to reach 90% of photosynthetic steady state; tP-steady, time required to reach 100% of photosynthetic steady state.

Fig. 7 Ribulose 1,5-bisphosphate carboxylation (RuBP) and regeneration capacity of Panax notoginseng leaves exposed to low-nitrogen (LN) and high-nitrogen (HN). D, Immunoblot analysis of 1,5-bisphosphate carboxylase (Rubisco), scenedesmus heptulose-1,7-bisphosphatase (SBPase) and fructose-1,6-bisphosphatase (FBPase), with the numbers on the right indicates the percentage of protein content of low-nitrogen leaves as a percentage of protein content of high-nitrogen leaves. Ci, intercellular CO2 concentration; Jmax, maximum rate of RuBP-regeneration; Pn, net photosynthetic rate; Vcmax, maximum carboxylation efficiency. * indicates significant differences between the two nitrogen treatments (p < 0.05).

Fig. 8 Enzyme activities of Panax notoginseng under steady-state and dynamic light conditions (mean ± SD). The bars at the top of each figure show the high light (800 μmol·m-2·s-1, white) and low light (50 μmol·m-2·s-1, grey) periods. Under irregular dynamic light condition (A, C, E), leaves were exposed under high light (800 μmol·m-2·s-1) condition for 20-40 min and then the leaves were exposed to low light (50 μmol·m-2·s-1) for 240 s and then the light was converted to high light for 120 s. Under regular dynamic light condition (B, D, F), leaves were treated with high light for 20-40 min, followed by alternating high light (800 μmol·m-2·s-1) and low light (50 μmol·m-2·s-1) every 120 s for 12 min. FBPase, fructose-1,6-bisphosphatase; Rubisco, 1,5-bisphosphate carboxylase; SBPase, scenedesmusheptulose-1,7-bisphosphatase. HN, high nitrogen; LN, low nitrogen. * indicates significant differences between the two nitrogen treatments (p < 0.05).

Fig. 9 High nitrogen (HN) exacerbates the decline of photosynthetic induction rate in a typically shade-tolerant species Panax notoginseng. The protein content of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in high-nitrogen leaves was higher than that of fructose-1,6-bisphosphatase (FBPase) and scenedesmus heptulose-1,7-bisphosphatase (SBPase); during the high light phase of dynamic light, HN leaves required activation of a higher proportion of FBPase and SBPase and a longer time to restore photosynthetic rate. The photosynthetic induction in the dynamic light of HN condition after low light interval was mainly limited by SBPase and FBPase reactivation rather than by Rubisco activity. The model shows the process of photosynthetic electron transfer, the red dashed line indicates that the process is fully activated and the green dashed line indicates that the process is inhibited, the red font indicates an increase in the amount (concentration) of the substance and the green font indicates a decrease in the amount (concentration) of the substance. ADP, adenosine diphosphate; ATP, adenosine triphosphate; OEC, oxygen-evolving complex; PC, plastocyanin; Pi, phosphate group; PSI, photosystem I; PSII, photosystem II. a, b, c, β, δ, α and ε, different subunits of ATP synthase; ADP, adenosine diphosphate; ATP, adenosine triphosphate; b6f, cytochrome b6-f complex; FBPase, fructose-1,6-bisphosphatase; Narea, N content per unit of leaf area; NADP+, nicotinamide adenine dinucleotide phosphate; OEC, oxygen-evolving complex; p680, chlorophyll II; p700, chlorophyl; PC, plastocyanin; Pi, phosphate group; PSI, photosystem I; PSII, photosystem II; RuBP, ribulose-1,5-disphosphate; Rubisco, ribulose-1,5-bisphosphate carboxylase; SBPase, sedoheptulose-1,7-bisphosphatase.

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