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CO2 uptake and chlorophyll a fluorescence of Suaeda fruticosa grown under diurnal rhythm and after transfer to continuous dark

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Abstract

Although only 2–4% of absorbed light is emitted as chlorophyll (Chl) a fluorescence, its measurement provides valuable information on photosynthesis of the plant, particularly of Photosystem II (PSII) and Photosystem I (PSI). In this paper, we have examined photosynthetic parameters of Suaeda fruticosa L. (family: Amaranthaceae), surviving under extreme xerohalophytic conditions, as influenced by diurnal rhythm or continuous dark condition. We report here CO2 gas exchange and the kinetics of Chl a fluorescence of S. fruticosa, made every 3 hours (hrs) for 3 days, using a portable infra-red gas analyzer and a Handy PEA fluorimeter. Our measurements on CO2 gas exchange show the maximum rate of photosynthesis to be at 08:00 hrs under diurnal condition and at 05:00 hrs under continuous dark. From the OJIP phase of Chl a fluorescence transient, we have inferred that the maximum quantum yield of PSII photochemistry must have increased during the night under diurnal rhythm, and between 11:00 and 17:00 hrs under constant dark. Overall, our study has revealed novel insights into how photosynthetic reactions are affected by the photoperiodic cycles in S. fruticosa under high salinity. This study has further revealed a unique strategy operating in this xero-halophyte where the repair mechanism for damaged PSII operates during the dark, which, we suggest, contributes to its ecological adaptation and ability to survive and reproduce under extreme saline, high light, and drought conditions. We expect these investigations to help in identifying key genes and pathways for raising crops for saline and dry areas.

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Abbreviations

Chl:

Chlorophyll

C i :

Internal CO2 concentration

EC:

Electrical conductivity

ETR:

Electron transport rate

F v/F m :

Maximum quantum yield of Photosystem II (PSII)

G s :

Stomatal conductance

hrs:

hours

NPQ:

Non-photochemical quenching of the excited state of Chl, usually by heat loss

NPR:

Net photosynthesis rate

q N :

A coefficient for non-photochemical quenching of the excited state of Chl

q P :

A coefficient for photochemical quenching of the excited state of Chl

ROS:

Reactive oxygen species

T r :

Transpiration rate

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Acknowledgements

SW, RJ, and RSR acknowledge Senior Research Fellowship from UGC (University Grants Commission, Government of India), Dr. D. S. Kothari Postdoctoral Fellowship from UGC, and DST-Inspire Doctoral Fellowship from DST (Department of Science and Technology), Government of India. Research in the Lab of AP is supported by funding from the Indo-US Science and Technology Forum (IUSSTF) for Indo-US Advanced Bioenergy Consortium (IUABC), International Atomic Energy Agency (Vienna), and UPE-II (India). Govindjee thanks the Departments of Plant Biology and Biochemistry of the University of Illinois at Urbana-Champaign for the use of computer facilities and office space. We thank Alexendrina Stirbet for reading this manuscript, especially Table 1.

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Authors and Affiliations

  1. Stress Physiology and Molecular Biology Laboratory, School of Life Sciences, Jawaharlal Nehru University, New Delhi, India

    Silas Wungrampha, Rohit Joshi & Ashwani Pareek

  2. Plant Stress Biology, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India

    Ray S. Rathore & Sneh L. Singla-Pareek

  3. Department of Biochemistry, Department of Plant Biology, and Center of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee

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  1. Silas Wungrampha
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  5. Govindjee
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SW, RJ, and RSR carried out the experiments. SW and RJ drafted the manuscript. AP conceived and designed the study. AP, SLS-P, and G finalized the manuscript. All the authors have read and approved the final manuscript.

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Correspondence to Ashwani Pareek.

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Supplementary material 1 (TIFF 576 kb) Supplementary Fig. 1 Light intensity at Sambhar Lake from dawn to dusk as on February of 2018 during the experimental period

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Supplementary material 2 (TIFF 344 kb) Supplementary Fig. 2 Percentage transmission from the double-layered black cloth that was used for covering plants to maintain continuous dark. Transmission from the dark cloth for the wavelength range of 300–900 nm was only ~ 1%

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Supplementary material 3 (TIFF 3033 kb) Supplementary Fig. 3 Polyphasic Chl a fluorescence transient of dark-adapted Suaeda fruticosa leaves at different intensities (2500–3400 μmol photons m−2 s−1) of 650 nm light a chlorophyll a fluorescence transient of the leaves of Suaeda fruticosa plotted on a logarithmic time scale. The O, J, I and P steps are marked in the figure, where, O is for origin (the minimum fluorescence Fo), J and I are for the intermediary fluorescence levels at 2 ms and 30 ms (Fj and Fi), and P is for the peak (Fp). b Fluorescence transients measured at different light intensities; the O–J–I–P transients shown here were normalized at Fo. c Variable fluorescence measured from the leaves of Suaeda fruticosa at different light intensities; the O–J–I–P fluorescence shown here were double normalized at Fo and Fm phase; V(t) = (F(t) − Fo)/(Fm − Fo)

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Supplementary material 4 (TIFF 3032 kb) Supplementary Fig. 4 Several photosynthetic parameters of photosynthesis of Suaeda fruticosa, as calculated from the data in Supplementary Fig. S3. a Quantum yield of the Photosystem II as inferred from the Chl a fluorescence (Fv/Fm), b ABS/RC, absorbed photon flux per an active PSII reaction center, c DIo/CSm, phenomenological energy flux dissipated per PSII cross section, d TRo/CSm, maximal trapped phenomenological energy flux per PSII cross section, e ETo/RC, the electron transport flux per active PSII reaction center and f performance index [PItotal = PIABS∙(1 − Vi)/(Vi − Vj)] for energy conservation from photons absorbed by PSII antenna, until the reduction of PSI acceptors

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Supplementary material 5 (TIFF 4963 kb) Supplementary Fig. 5 Photosynthetic parameters of Suaeda fruticosa under diurnal condition for the first 24 hrs followed by continuous dark for the following 48 hrs. Using IRGA, photosynthetic parameters at the different time point of the day were measured from the leaves of S. fruticosa for 72 hrs (3 days). The shaded portion of the graph represents night. To maintain continuous dark, the plant was completely covered with a dark cloth. A clear rhythmic activity that repeats every 24 hrs was seen in all the parameters. a Stomatal conductivity, b net photosynthesis rate, c a quotient for photochemical quenching of the excited state of Chl, d a quotient for non-photochemical quenching of the excited state of Chl, e internal carbon dioxide concentration, f non-photochemical quenching of the excited state of Chl, usually by heat loss, g electron transport rate, h transpiration rate and i quantum yield of Photosystem II as inferred from Chl a fluorescence

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Supplementary material 6 (TIFF 1825 kb) Supplementary Fig. 6 Comparison of the OJIP transient curve between Suaeda fruticosa leaves under diurnal (full line) and continuous dark (broken line) at different time points. At all the time points, the observed parameters showed that the continuous dark and the diurnal clock of Suaeda differ from each other

Supplementary material 7 (DOCX 18 kb)

Supplementary material 8 (DOCX 19 kb)

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Wungrampha, S., Joshi, R., Rathore, R.S. et al. CO2 uptake and chlorophyll a fluorescence of Suaeda fruticosa grown under diurnal rhythm and after transfer to continuous dark. Photosynth Res 142, 211–227 (2019). https://doi.org/10.1007/s11120-019-00659-0

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