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High nitrogen inhibits photosynthetic performance in a shade-tolerant and N-sensitive species Panax notoginseng

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Abstract

Nitrogen (N) is a primary factor limiting leaf photosynthesis. However, the mechanism of high-N-driven inhibition on photosynthetic efficiency and photoprotection is still unclear in the shade-tolerant and N-sensitive species such as Panax notoginseng. Leaf chlorophyll (Chl) content, Ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) activity and content, N allocation in the photosynthetic apparatus, photosynthetic performance and Chl fluorescence were comparatively analyzed in a shade-tolerant and N-sensitive species P. notoginseng grown under the levels of moderate nitrogen (MN) and high nitrogen (HN). The results showed that Rubisco content, Chl content and specific leaf nitrogen (SLN) were greater in the HN individuals. Rubisco activity, net photosynthetic rate (Anet), photosynthetic N use efficiency (PNUE), maximum carboxylation rate (Vcmax) and maximum electron transport rate (Jmax) were lower when plants were exposed to HN as compared with ones to MN. A large proportion of leaf N was allocated to the carboxylation component under the levels of MN. More N was only served as a form of N storage and not contributed to photosynthesis in HN individuals. Compared with the MN plants, the maximum quantum yield of photosystem II (Fv/Fm), non-photochemical quenching of PSII (NPQ), effective quantum yield and electron transport rate were obviously reduced in the HN plants. Cycle electron flow (CEF) was considerably enhanced in the MN individuals. There was not a significant difference in maximum photo-oxidation P700+ (Pm) between the HN and MN individuals. Most importantly, the HN individuals showed higher K phase in the fast chlorophyll fluorescence induction kinetic curve (OJIP kinetic curve) than the MN ones. The results obtained suggest that photosynthetic capacity might be primarily inhibited by the inactivated Rubisco in the HN individuals, and HN-induced depression of photoprotection might be caused by the photodamage to the donor side of PSII oxygen-evolving complex.

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Abbreviations

A net :

Net photosynthetic rate

A max :

Maximum net photosynthetic assimilation under saturating light

AQY:

Apparent quantum efficiency

BSA:

Bovine serum albumin

C i :

Internal leaf CO2 concentrations

Cond:

Stomatal conductance

C c :

Leaf Chl concentration

C B :

Ratio of chlorophyll to organic leaf N in light capture components

Chl:

Leaf chlorophyll

Chla :

Chlorophyll a

Chlb :

Chlorophyll b

CEF:

Cycle electron flow

CE:

Carboxylation efficiency

ETRI:

Electron transport rate of PSI

ETRII:

Electron transport rate of PSII

F o :

Minimum fluorescence after dark adaptation

F m :

Maximum fluorescence after dark adaptation

F o′:

Minimum fluorescence after light adaptation

F m′:

Maximum fluorescence after light adaptation

F s :

Light-adapted steady-state fluorescence

F t :

Relative fluorescence intensity at different points of time

F v/F m :

Maximum quantum yield of photosystem II

HN:

High nitrogen

Γ*:

CO2 compensation point

J mc :

Potential rate of photosynthetic electron transport per unit cyt f

J max :

Maximum electron transfer rate

LEF:

Linear electron transport

LHCII:

Light capture complex of PSII

LSP:

Light saturation point

LCP:

Light compensation point

MN:

Moderate nitrogen

N:

Nitrogen

N lc :

Nitrogen content in light capture component

N cb :

Nitrogen content in carboxylation component

N et :

Nitrogen content of electron transport components

N psn :

Photosynthetic nitrogen content

N non-psn :

Non-photosynthetic nitrogen content

NPQ:

Non-photochemical quenching in PSII

OJIP:

Fast chlorophyll fluorescence induction kinetic curve

OEC:

Oxygen-evolving complex

PSI:

Photosystem I

PSII:

Photosystem II

PAR:

Photosynthetic active radiation

P non-psn :

Coefficients for leaf nitrogen partitioning in non-photosynthetic components

P psn :

Coefficients for leaf nitrogen partitioning in photosynthetic components

P lc :

Coefficients for leaf nitrogen partitioning into light capture component

P cb :

Coefficients for leaf nitrogen partitioning into carboxylation component

P et :

Coefficients for leaf nitrogen partitioning into electron transport component

PNUE:

Photosynthetic nitrogen use efficiency

P :

P700+ signals

P m :

Maximum photo-oxidation P700+

ROS:

Reactive oxygen species

Rubisco:

Ribulose-1,5-bisphosphate carboxylase oxygenase

R d :

Dark respiration rate

R L :

Light respiration rate

SLN:

Specific leaf nitrogen

V cr :

Specific activity of Rubisco

V t :

Relative variable fluorescence intensity

V cmax :

Maximum carboxylation rate

W K :

The ratio of the variable fluorescent FK occupying the FJ-FO amplitude

Y(I):

Quantum yield of PSI

Y(ND):

Donor side limitation of PSI

Y(NA):

Acceptor side limitation of PSI

Y(II):

Effective quantum yield of PSII photochemistry

Y(NPQ):

Yield of regulated energy dissipation of PSII

Y(NO):

Yield of non-regulated energy dissipation of PSII

1-qP :

Redox poise of the primary electron acceptor of PSII

∆pH:

Proton gradient across the thylakoid membranes

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Acknowledgements

We are grateful to Sheng-Pu Shuang and Rong-Mei Huang for their assistance with data analysis and field experiment.

Funding

This work was supported by the National Natural Science Foundation of China (Grant number 81360609 and 81860676). In addition, this work was also supported by the Major Special Science and Technology Project of Yunnan Province (2016ZF001 and 2017ZF001). All authors have read and approved the current version of the manuscript.

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All authors contribute to the conception and design of the study. J-W C conceived the study, and Z C designed the experiments and wrote the manuscript; the experimental measurement was completed by Z C, J-Y Z and H-M W. J-Y Z, H-M W and L Z carried out the analysis. All authors have read and approved the current version of the manuscript.

Corresponding author

Correspondence to Jun-Wen Chen.

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The authors declare that they have no conflicts of interest.

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Cun, Z., Zhang, JY., Wu, HM. et al. High nitrogen inhibits photosynthetic performance in a shade-tolerant and N-sensitive species Panax notoginseng. Photosynth Res 147, 283–300 (2021). https://doi.org/10.1007/s11120-021-00823-5

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  • DOI: https://doi.org/10.1007/s11120-021-00823-5

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