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Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities

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Abstract

Arabidopsis plants grown at low light were exposed to a gradually increasing actinic light routine. This method allows for the discerning of the photoprotective component of NPQ, pNPQ and photoinhibition. They exhibited lower values of Photosystem II (PSII) yield in comparison to high-light grown plants, and higher calculated dark fluorescence level (F′o calc.) than the measured one (F′o act.). As a result, in low-light grown plants, the values of qP measured in the dark appeared higher than 1. Normally, F′o act. and F′o calc. match well at moderate light intensities but F′o act. becomes higher at increasing intensities due to reaction centre (RCII) damage; this indicates the onset of photoinhibition. To explain the unusual increase of qP in the dark in low-light grown plants, we have undertaken an analysis of PSII antenna size using biochemical and spectroscopic approaches. Sucrose gradient separation of thylakoid membrane complexes and fast fluorescence induction experiments illustrated that the relative PSII cross section does not increase appreciably with the rise in PSII antenna size in the low-light grown plants. This suggests that part of the increased LHCII antenna is less efficiently coupled to the RCII. A model based upon the existence of an uncoupled population LHCII is proposed to explain the discrepancies in calculated and measured values of F′o.

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Acknowledgments

We would like to thank Professor Leonas Valkunas and Dr Christopher Duffy for helpful discussions. This work was supported by Queen Mary Principal’s research studentship to MAW and The Leverhulme Trust and UK Biotechnology and Biological Sciences Research Council to AVR.

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    Maxwell A. Ware, Erica Belgio & Alexander V. Ruban

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11120_2015_102_MOESM1_ESM.pptx

Supplementary materialFig. S1 a Typical high light acclimated plant chlorophyll fluorescence scheme of induction with an eight step increasing actinic light (AL) routine. In this example 0, 90, 190, 280, 420, 625, 820, 1150, and 1500 µmol m−2 s−1 AL intensities were used. 80 and 90 % AL intensities of the aforesaid values were achieved by carefully extracting the fibre-optic from the emitting diode and determining the AL intensity with a Walz MQS-B sensor. This allowed a more accurate reflection of PSII susceptibility to photodamage to be realised. For a detailed explanation of routine development see Ruban and Belgio (2014). b A zoomed in region of the fluorescence scheme (a) illustrating the timing and application of 625, 820 and 1150 µmol m−2 s−1 AL (upward arrow and downward arrow demonstrate the turning of AL on and off, respectively), along with saturating pulses (SP) (P1, P2, P3). P1 indicates an SP in the dark, or after 10 s of far red (FR) light, P2 during AL illumination, and P3 at the end of AL treatment. The difference between Fo′act. and Fo′calc. is determined at P1, and subsequently used to calculate qPd. At low AL intensities, there is little to no difference between Fo′calc. and Fo′act., but under increasing AL intensities, the two values diverge. See also ‘Materials and methods’ for a detailed description. The timing scheme in the dark was (AL off)(FR on)-(10 s)-(FR off/SP)-(5 s)-(AL on).Fig. S2 a ΔFo′ [(Fo′act.-Fo′calc.)/Fo′act.] results obtained from fluorescence traces for each AL intensity were averaged for medium-light grown plants. Error bars show SEM (n = 10). b Relationship between NPQ and qPd (open circles) and NPQ and PSII actual yield (closed circles) for medium-light grown plants. Data points were averaged from 30 repeats on whole intact leaves. Error bars show the standard error of the mean (n = 30). The theoretical yield (continuous line) was calculated using Eq. 1 of ‘Materials and methods’, but with qPd always equal to 1.Fig. S3 Absorbance spectra (Hitachi, U-3310 spectrophotometer) conducted on bands obtained from sucrose gradients (Fig. 4) for (a) low-light (b) medium-light (c) high-light grown plants. All bands were zeroed at 750 nm. Band 2–5 correspond to monomers, trimeric LHCII, LHCII-CP29-CP24, PSII core complexes, respectively. Bands 1 and 6 were identified as free pigments and PSI-LHCI, respectively (data not shown).Fig. S4Example of calculation of integral below absorbance spectra taken from Fig. S3 (band 5), with trace zeroed at 750 nm. Using OriginPro 9.0, the mathematical area under each trace was calculated using the integrate function between 550 and 750 nm. This area was used to calculate the total amount of arbitrary chlorophyll. This was achieved by multiplying the total amount of the band extraction from the sucrose gradient (ml) by the dilution factor of solution used to perform the absorbance spectra, and by the area measured under the trace. This arbitrary chlorophyll value was divided by the number of chlorophylls per complex in each band (42 chlorophylls per LHCII trimer (band 3), 66 per LHCII-CP29-CP24 complex (band 4) and 35 per PSII core complex (band 5) to ascertain the amount of complexes present.Fig. S5PSII fast fluorescence induction traces performed on detached lincomycin-treated leaves. Vacuum infiltration with 30 μM DCMU was perfomed 20 s before exposure to 7 μmol m-2 s-1. Traces are the mean values for 3 repeats. All traces were zeroed at Fo and normalised to 1 at F m .Fig. S6The average qPd value for HL, ML and LL grown plants at the end of all gradually increasing actinic light routines. 10 repeats of each (0, 90, 190, 280, 420, 625, 820, 1150, 1500 µmol m−2 s−1) (0, 81, 171, 256.5, 378, 562.5, 738, 1035, 1350 µmol m−2 s−1) (0, 72, 152, 228, 336, 500, 656, 920, 1200 µmol m−2 s−1) incrementing routines were performed. Error bars illustrate the standard error of the mean (n = 30).Supplementary material 1 (PPTX 417 kb)

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Ware, M.A., Belgio, E. & Ruban, A.V. Photoprotective capacity of non-photochemical quenching in plants acclimated to different light intensities. Photosynth Res 126, 261–274 (2015). https://doi.org/10.1007/s11120-015-0102-4

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