Photosynthesis Research

, Volume 141, Issue 3, pp 315–330 | Cite as

Dynamics of regulated YNPQ and non-regulated YNO energy dissipation in sunflower leaves exposed to sinusoidal lights

  • Guy SamsonEmail author
  • Laurianne Bonin
  • Vincent Maire
Original Article


Better understanding of photosynthetic efficiency under fluctuating light requires a specific approach to characterize the dynamics of energy dissipation in photosystem II. In this study, we characterized the interaction between the regulated YNPQ and non-regulated YNO energy dissipation in outdoor- and indoor-grown sunflower leaves exposed to repetitive cycles of sinusoidal lights of five amplitudes (200, 400, 600, 800, 1000 µmol m−2 s−1) and periods (20, 40, 60, 90, 120 s). The different light cycles induced various patterns of ChlF emission, from which were calculated the complementary quantum yields of photochemical energy conversion YII, light-regulated YNPQ, and non-regulated YNO non-photochemical energy dissipation. During the light cycles, YNO varied in complex but small patterns relative to those of YNPQ, whose variations were mostly mirrored by changes in YII. The YNO patterns could be decomposed by fast Fourier transform into a main (MH) and several upper harmonics (UH). Concerning YNPQ dynamics, they were described by sinusoidal regressions with two components, one constant during the light cycles but increasing with the average light intensity (YNPQc), and one variable (YNPQv). Formation and relaxation of YNPQv followed the intensity of the sinusoidal lights, with lags ranging from 5 to 13 s. These lags decreased with the amplitude of the incident light, and were shorter by 37% in outdoor than indoor leaves. YNPQv and UHs responses to the growth conditions, amplitudes, and the periods of the sinusoidal light were closely correlated (r = 0.939), whereas MH and YNPQc varied similarly (r = 0.803). The analysis of ChlF induced by sinusoidal lights may be a useful tool to better understand the dynamics of energy dissipation in PSII under fluctuating lights.


Energy allocation Fluctuating light Photosystem II PsbS protein qE Zeaxanthin 



Chlorophyll a fluorescence


Fast Fourier transform




Main (first) harmonic of the ChlF patterns induced by sinusoidal lights


Sum of the amplitudes of the upper harmonics (n ≤ 2) of the ChlF patterns induced by sinusoidal lights


Photon flux density


Photosystem II, photosystem I


Quantum yield of photochemical energy conversion in PS II


Quantum yield of light-regulated non-photochemical energy dissipation in PS II


Quantum yield of non-regulated non-photochemical energy dissipation in PS II


Constant and variable portions of YNPQ measured during a cycle of sinusoidal light



A financial support from the Groupe de Recherche en Biologie Végétale of the Université du Québec à Trois-Rivières is gratefully acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_633_MOESM1_ESM.docx (371 kb)
Supplementary material 1 (DOCX 371 KB)


  1. Alter P, Dreissen A, Luo FL, Matsubara S (2012) Acclimatory responses of Arabidopsis to fluctuating light environment: comparison of different sunfleck regimes and accessions. Photosynth Res 113:221–237. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. CrossRefGoogle Scholar
  4. Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta Bioenerg 1847:468–485. CrossRefGoogle Scholar
  5. Endo T, Uebayashi N, Ishida S, Ikeuchi M, Sato F (2014) Light energy allocation at PSII under field light conditions: how much energy is lost in NPQ-associated dissipation? Plant Physiol Biochem 81:115–120. CrossRefPubMedGoogle Scholar
  6. Grobbelaar JU, Nedbal L, Tichý V (1996) Influence of high frequency light/dark fluctuations on photosynthetic characteristics of microalgae photoacclimated to different light intensities and implications for mass algal cultivation. J Appl Phycol 8:335–343. CrossRefGoogle Scholar
  7. Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81. CrossRefPubMedGoogle Scholar
  8. Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375–385CrossRefPubMedGoogle Scholar
  9. Ikeuchi M, Uebayashi N, Sato F, Endo T (2014) Physiological functions of PsbS-dependent and PsbS-independent NPQ under naturally fluctuating light conditions. Plant Cell Physiol 55:1286–1295. CrossRefPubMedGoogle Scholar
  10. Jishi T, Matsuda R, Fujiwara K (2015) A kinetic model for estimating net photosynthetic rates of cos lettuce leaves under pulsed light. Photosynth Res 124:107–116. CrossRefPubMedGoogle Scholar
  11. Joliot PA, Finazzi G (2010) Proton equilibration in the chloroplast modulates multiphasic kinetics of nonphotochemical quenching of fluorescence in plants. Proc Natl Acad Sci USA 107:12728–12733. CrossRefPubMedGoogle Scholar
  12. Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta Bioenerg 1757:362–368. CrossRefGoogle Scholar
  13. Kaiser E, Morales A, Harbinson J, Kromdijk J, Heuvelink E, Marcelis LFM (2015) Dynamic photosynthesis in different environmental conditions. J Exp Bot 66:2415–2426. CrossRefPubMedGoogle Scholar
  14. Kaiser E, Morales A, Harbinson J (2018) Fluctuating light takes crop photosynthesis on a rollercoaster ride. Plant Physiol 176:977–989. CrossRefPubMedGoogle Scholar
  15. Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Appl Notes 1:27–35Google Scholar
  16. Kono M, Terashima I (2014) Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J Photochem Photobiol B 137:89–99. CrossRefPubMedGoogle Scholar
  17. Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004. CrossRefPubMedGoogle Scholar
  18. Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861. CrossRefPubMedGoogle Scholar
  19. Külheim C, Jansson S (2005) What leads to reduced fitness in non-photochemical quenching mutants? Physiol Plant 125:202–211. CrossRefGoogle Scholar
  20. Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93. CrossRefPubMedGoogle Scholar
  21. Küppers M, Pfiz M (2009) Role of photosynthetic induction for daily and annual carbon gains of leaves and plant canopies. In: Laisk A, Nedbal L, Govindjee (eds) Photosynthesis in silico. Understanding complexity from molecules to ecosystems. Springer, Dordrecht, pp 417–440CrossRefGoogle Scholar
  22. Laisk A, Oja V, Rasulov B, Eichelmann H, Sumberg A (1997) Quantum yields and rate constants of photochemical and nonphotochemical excitation quenching: experiment and model. Plant Physiol 115:803–815. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lawson T, Kramer DM, Raines CA (2012) Improving yield by exploiting mechanisms underlying natural variation of photosynthesis. Curr Opin Biotechnol 23:215–220. CrossRefPubMedGoogle Scholar
  24. Nedbal L, Březina V (2002) Complex metabolic oscillations in plants forced by harmonic irradiance. Biophys J 83:2180–2189. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Nedbal L, Březina V, Adamec F, Štys D, Oja V, Laisk A, Govindjee (2003) Negative feedback regulation is responsible for the non-linear modulation of photosynthetic activity in plants and cyanobacteria exposed to a dynamic light environment. Biochim Biophys Acta Bioenerg 1607:5–17. CrossRefGoogle Scholar
  26. Nedbal L, Březina V, Červený J, Trtílek M (2005) Photosynthesis in dynamic light: systems biology of unconventional chlorophyll fluorescence transients in Synechocystis sp. PCC 6803. Photosynth Res 84:99–106. CrossRefPubMedGoogle Scholar
  27. Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta Bioenerg 1797:466–475. CrossRefGoogle Scholar
  28. Pearcy RW (1983) The light environment and growth of C3 and C4 tree species in the understory of a Hawaiian forest. Oecologia 58:19–25. CrossRefPubMedGoogle Scholar
  29. Prášil O, Kolber ZS, Falkowski PG (2018) Control of the maximal chlorophyll fluorescence yield by the QB binding site. Photosynthetica 56(1):150–162. CrossRefGoogle Scholar
  30. Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170:1903–1916. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Samson G, Bruce D (1996) Origins of the low-yield of chlorophyll-a fluorescence induced by single turnover flash in spinach thylakoids. Biochim Biophys Acta Bioenerg 1276:147–153CrossRefGoogle Scholar
  32. Schindler C, Lichtenthaler HK (1996) Photosynthetic CO2-assimilation, chlorophyll fluorescence and zeaxanthin accumulation in field-grown maple trees in the course of a sunny and a cloudy day. J Plant Physiol 148:399–412CrossRefGoogle Scholar
  33. Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Schumann T, Paul S, Melzer M, Dörmann P, Jahns P (2017) Plant growth under natural light conditions provides highly flexible short-term acclimation properties toward high light stress. Front Plant Sci. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem i in sunflower leaves. Plant Cell Physiol 55:1184–1193. CrossRefPubMedGoogle Scholar
  36. Slattery RA, Walker BJ, Weber APM, Ort DR (2018) The impacts of fluctuating light on crop performance. Plant Physiol 176:990–1003. CrossRefPubMedGoogle Scholar
  37. Stegemann J, Timm H-C, Küppers M (1999) Simulation of photosynthetic plasticity in response to highly fluctuating light: an empirical model integrating dynamic photosynthetic induction and capacity. Trees Struct Funct 14:145–160. CrossRefGoogle Scholar
  38. Stramski D, Legendre L (1992) Laboratory simulation of light-focusing by water-surface waves. Mar Biol 114:341–348CrossRefGoogle Scholar
  39. Sylak-Glassman EJ, Malnoe A, De Re E, Brooks MD, Fischer AL, Krishna K, Fleming GR (2014) Distinct roles of the photosystem II protein PsbS and zeaxanthin in the regulation of light harvesting in plants revealed by fluorescence lifetime snapshots. Proc Natl Acad Sci USA 111:17498–17503. CrossRefPubMedGoogle Scholar
  40. Taylor SH, Long SP (2017) Slow induction of photosynthesis on shade to sun transitions in wheat may cost at least 21% of productivity. Philos Trans R Soc B 372:1730. CrossRefGoogle Scholar
  41. Tennessen DJ, Bula RJ, Sharkey TD (1995) Efficiency of photosynthesis in continuous and pulsed light emitting diode irradiation. Photosynth Res 44:261–269. CrossRefPubMedGoogle Scholar
  42. Tikkanen M, Grebe S (2018) Switching off photoprotection of photosystem I—a novel tool for gradual PSI photoinhibition. Physiol Plant 162:156–161. CrossRefPubMedGoogle Scholar
  43. Tóth SZ, Schansker G, Strasser RJ (2005) In intact leaves, the maximum fluorescence level (FM) is independent of the redox state of the plastoquinone pool: a DCMU-inhibition study. Biochim Biophys Acta Bioenerg 1708:275–282. CrossRefGoogle Scholar
  44. Tsuyama M, Kobayashi Y (2009) Reduction of the primary donor P700 of photosystem I during steady-state photosynthesis under low light in Arabidopsis. Photosynth Res 99:37–47. CrossRefPubMedGoogle Scholar
  45. Vernotte C, Etienne AL, Briantais J-M (1979) Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochim Biophys Acta 545:519–527CrossRefPubMedGoogle Scholar
  46. Vialet-Chabrand S, Matthews JSA, Simkin AJ, Raines CA, Lawson T (2017) Importance of fluctuations in light on plant photosynthetic acclimation. Plant Physiol 173:2163–2179. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Xu X, Liu J, Shi Q, Mei H, Zhao Y, Wu H (2016) Ocean warming alters photosynthetic responses of diatom Phaeodactylum tricornutum to fluctuating irradiance. Phycologia 55:126–133. CrossRefGoogle Scholar
  48. Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zaks J, Amarnath K, Kramer DM, Niyogi KK, Fleming GR (2012) A kinetic model of rapidly reversible nonphotochemical quenching. Proc Natl Acad Sci USA 109:15757–15762. CrossRefPubMedGoogle Scholar
  50. Zhu X-G, Ort DR, Whitmarsh J, Long SP (2004) The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. J Exp Bot 55:1167–1175CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Département des sciences de l’environnement, Groupe de recherche en biologie végétale (GRBV)Université du Québec à Trois-Rivières (UQTR)Trois-RivièresCanada

Personalised recommendations