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Changes in the photosynthesis properties and photoprotection capacity in rice (Oryza sativa) grown under red, blue, or white light

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Abstract

Non-photochemical quenching (NPQ) of the excited state of chlorophyll a is a major photoprotective mechanism plants utilize to survive under high light. Here, we report the impact of long-term light quality treatment on photosynthetic properties, especially NPQ in rice. We used three LED-based light regimes, i.e., red (648–672 nm), blue (438–460 nm), and “warm” white light (529–624 nm), with the incident photon flux density of 300 µmol photons m−2 s−1, the difference in the absorbed photon flux densities by leaves grown under different light quality being less than 7%. Our results show that blue light, as compared to white light, induced a significant decrease in Fv/Fm, a decreased rate of reduction of P700+ after P700 was completely oxidized; furthermore, blue light also induced higher NPQ with an increased initial speed of NPQ induction, which corresponds to the qE component of NPQ, and a lower maximum quantum yield of PSII, i.e., Y(II). In contrast, rice grown under long-term red light showed decreased Y(II) and increased NPQ, but with no change in Fv/Fm. Furthermore, we found that rice grown under either blue or red light showed decreased transcript abundance of both catalase and ascorbate peroxidase, together with an increased H2O2 content, as compared to rice grown under white light. All these data suggest that even under a moderate incident light level, rice grown under blue or red light led to compromised antioxidant system, which contributed to decreased quantum yield of photosystem II and increased NPQ.

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References

  • Alboresi A, DallOsto L, Aprile A, Carillo P, Roncaglia E, Cattivelli L, Bassi R (2011) Reactive oxygen species and transcript analysis upon excess light treatment in wild-type Arabidopsis thaliana vs a photosensitive mutant lacking zeaxanthin and lutein. BMC Plant Biol 11:62–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their function. Plant Physiol 141:391–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beauchemin R, Gauthier A, Harnois J, Boisvert S, Govindachary S, Carpentier R (2007) Spermine and spermidine inhibition of photosystem II: disassembly of the oxygen evolving complex and consequent perturbation in electron donation from TyrZ to P680 + and the quinone acceptors QA to QB. Biochim Biophys Acta 1767:905–912

    Article  CAS  PubMed  Google Scholar 

  • Belgiol E, Trsková E, Kotabová E, Ewe D, Prášil O, Kaňa R (2018) High light acclimation of Chromera velia points to photoprotective NPQ. Photosynth Res 135:263–274

    Article  CAS  Google Scholar 

  • Bian Z, Yang Q, Lib T, Cheng R, Barnetta Y, Lua C (2018) Study of the beneficial effects of green light on lettuce grown under short-term continuous red and blue light-emitting diodes. Physiol Plant. http://irep.ntu.ac.uk/id/eprint/33129

  • Björkman O, Powles SB (1987) Leaf movement in the shade species Oxalis oregana L I. Response to light level and light quality. Carnegie Inst Wash Year Book 80:59–62

    Google Scholar 

  • Bukhov NG, Drozdova IS, Bondar VV (1995) Light response curves of photosynthesis in leaves of sun-type and shade-type plants grown in blue or red light. J Photochem Photobiol B 30:39–41

    Article  CAS  Google Scholar 

  • Cazzaniga S, Osto LD, Kong SG, Wada M, Bassi R (2013) Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. Plant J 76:568–579

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto L, Caffarri S, Bassi R (2005) A mechanism of nonphotochemical energy dissipation, independent from Psbs, revealed by a conformational change in the antenna protein CP26. Plant Cell 17:1217–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio Protoc 2(18):1–4

    Article  Google Scholar 

  • Demmig-Adams B, Garab G, Adams WW, Govindjee (eds) (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht

    Google Scholar 

  • 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 1847:468–485

    Article  CAS  PubMed  Google Scholar 

  • Eskins K, Jiang CZ, Shibles R (1991) Light-quality and irradiance effects on pigments, light-harvesting proteins and Rubisco activity in a chlorophyll- and light-harvesting-deficient soybean mutant. Physiol Plant 83:47–53

    Article  CAS  Google Scholar 

  • Evans JR (1989) Partitioning of nitrogen between and within leaves grown under different irradiances. Aust J Plant Physiol 16:533–548

    Google Scholar 

  • Fratanico A, Tocquin P, Franck F (2016) The chlorophyll a fluorescence induction curve in the green microalga Haematococcus pluvialis: further insight into the nature of the P-S-M fluctuation and its relationship with the “low wave” phenomenon sat steady state. Photosynth Res 128:271–285

    Article  CAS  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    CAS  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Glick RE, McCauley SW, Gruissem W, Melis A (1986) Light quality regulates expression of choloroplast genes and assembly of photosynthetic membrane complexes. Proc Natl Acad Sci USA 83:4287–4291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant RH (1997) Partitioning of biologically active radiation in plant canopies. Int J Biometeorol 40:26–40

    Article  Google Scholar 

  • Green BR, Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 47:685–714

    Article  CAS  Google Scholar 

  • Green BR, Parson WW (eds) (2003) Light-harvesting antennas in photosynthesis. Springer, Dordrecht

    Google Scholar 

  • Gyula P, Schäfer E, Nagy F (2003) Light perception and signalling in higher plants. Curr Opin Plant Biol 6:446–452

    Article  CAS  PubMed  Google Scholar 

  • Hamdani S, Carpentier R (2009) Interaction of methylamine with extrinsic and intrinsic subunits of photosystem II. Biochim Biophys Acta 1787:1223–1229

    Article  CAS  PubMed  Google Scholar 

  • Hamdani S, Qu M, Xin CP, Li M, Chu C, Govindjee Zhu XG (2015) Variations between the photosynthetic properties of elite and landrace Chinese rice cultivars revealed by simultaneous measurements of 820 nm transmission signal and chlorophyll a fluorescence induction. J Plant Physiol 177:128–138

    Article  CAS  PubMed  Google Scholar 

  • Hasni I, Hamdani S, Carpentier R (2013) Destabilization of the oxygen evolving complex of photosystem II by Al3+. Photochem Photobiol 89:1135–1142

    Article  CAS  PubMed  Google Scholar 

  • Hogewoning SW, Trouwborst G, Maljaars H, Poorter H, Ieperen WV, Harbinson J (2010) Blue light dose–responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. J Exp Bot 61:3107–3117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holm G (1954) Chlorophyll mutations in barley. Acta Agric Sci 4:457–461

    Article  Google Scholar 

  • Huang W, Tikkanen M, Zhang SB (2018) Photoinhibition of photosystem I in Nephrolepis falciformis depends on reactive oxygen species generated in the chloroplast stroma. Photosynth Res 137:129–140

    Article  CAS  PubMed  Google Scholar 

  • Inada K (1980) Spectral absorption property of pigments in living leaves and its contribution to photosynthesis. Japan Jour Crop Sci 49:286–294

    Article  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Lett 582:262–266

    Article  CAS  PubMed  Google Scholar 

  • Jung ES, Lee S, Lim SH, Ha SH, Liu KH, Lee CH (2013) Metabolite profiling of the short-term responses of rice leaves (Oryza sativa cv. Ilmi) cultivated under different LED lights and its correlations with antioxidant activities. Plant Sci 210:61–69

    Article  CAS  PubMed  Google Scholar 

  • Kagawa T, Wada M (2000) Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. Plant Cell Physiol 41:84–93

    Article  CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Kodru S, Malavath T, Devadasu E, Nellaepalli S, Stirbet A, Subramanyam R, Govindjee (2015) The slow S to M rise of chlorophyll a fluorescence reflects transitions from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth Res 125:219–231

    Article  CAS  PubMed  Google Scholar 

  • Koller D (1990) Light-driven leaf movements. Plant Cell Environ 13:615–632

    Article  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New flux parameters for the determination of QA redox state and excitation fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Kromdijk J, Glowacka 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

    Article  CAS  PubMed  Google Scholar 

  • Leonelli L, Brooks MD, Niyogi KK (2017) Engineering the lutein epoxide cycle into Arabidopsis thaliana. Proc Natl Acad Sci USA 114:7002–7008

    Article  CAS  Google Scholar 

  • Leong TY, Anderson JM (1984) Effect of light quality on the composition and function of thylakoid membranes in Atriplex triangularis. Biochim Biophys Acta 766:533–541

    Article  CAS  Google Scholar 

  • Leong TY, Goodchild DJ, Anderson JM (1985) Effect of light quality on the composition, function, and structure of photosynthetic thylakoid membranes of Asplenium australasicum (Sm.). Hook Plant Physiol 78:561–567

    Article  CAS  PubMed  Google Scholar 

  • Livak K, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Melis A, Spangfort M, Andersson B (1987) Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts. Photochem Photobiol 45:129–136

    Article  CAS  Google Scholar 

  • Miyake C, Horiguchi S, Makino A, Shizaki Y, Yamamoto H, Tomizawa KI (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830

    Article  CAS  PubMed  Google Scholar 

  • Möglich A, Yang X, Ayers RA, Moffat K (2010) Structure and function of plant photoreceptors. Ann Review Plant Biol 61:21–47

    Article  CAS  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    Article  CAS  Google Scholar 

  • Nilkens M, Kress E, Lambrev P, Milosalvina 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 1797:466–475

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  CAS  Google Scholar 

  • Norcini JG, Andersen PC, Knox GW (1991) Light intensity influences leaf physiology and plant growth characteristics of Photinia × fraseri. J Am Hort Sci 116:1046–1051

    Article  Google Scholar 

  • Oguchi R, Douwstara P, Fujita T, Chow WS, Terashima I (2011) Intra-leaf gradients of photoinhibition induced by different color lights: implications for the dual mechanisms of photoinhibition and for the application of conventional chlorophyll fluorometers. New Phytol 191:146–159

    Article  PubMed  Google Scholar 

  • Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama N, Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44:8494–8499

    Article  CAS  PubMed  Google Scholar 

  • Ort DR (2001) When there is too much light. Plant Physiol 125:29–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papageorgiou GC, Govindjee (2011) Photosystem II fluorescence: slow changes—scaling from the past. J Photochem Photbiol B 104:258–270

    Article  CAS  Google Scholar 

  • Papageorgiou GC, Govindjee (2014) The non-photochemical quenching of the electronically excited state of chlorophyll a in plants: definitions, timeline, viewpoints. Open questions. In: Demmig B, Adams G, Garab WW, Adams III, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. advances in photosynthesis and respiration including bioenergy and related processes. Springer, Dordrecht

    Google Scholar 

  • Pfündel E, Klughammer C, Schreiber U (2008) Monitoring the effects of reduced PSII antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Appl Notes 1:21–24

    Google Scholar 

  • Porra RJ, Thompson WA, Kriedelman PE (1989) Determination of accurate extraction and simultaneously equation for assaying chlorophyll a and b extracted with different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta -Bioenerg 1787:1151–1160

    Article  CAS  Google Scholar 

  • Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218–231

    Article  CAS  PubMed  Google Scholar 

  • Pospíšil P, Prasad A (2014) Formation of singlet oxygen and protection against its oxidative damage in photosystem II under abiotic stress. J Photochem Photobiol B 137:39–48

    Article  CAS  PubMed  Google Scholar 

  • Rochaix J (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV (2018) Light harvesting control in plants. FEBS Lett. https://doi.org/10.1002/1873-3468.13111

    Article  PubMed  Google Scholar 

  • Rubin AV, Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotchemical energy dissipation in isolated light harvesting complexes, intact chloroplasts and leaves of spinach. Plant Physiol 119:531–542

    Article  Google Scholar 

  • Sacharz J, Giovagnetti V, Ungerer P, Mastroianni G, Ruban A (2017) The xanthophyll cycle affects reversible PsbS-LHCII interactions to control non-photochemical quenching. Nat Plants 3:16225–16234

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U (2004) Pulse amplitude modulation fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. advances in photosynthesis and respiration including bioenergy and related processes. Springer, Dordrecht

    Google Scholar 

  • Senger H, Bauer B (1987) The influence of light quality on adaptation and function of the photosynthetic apparatus. Photochem Photobiol 45:939–946

    Article  CAS  Google Scholar 

  • Sztatelman O, Waloszek A, Banas AK, Gabrys H (2010) Photoprotective function of chloroplast avoidance movement: in vivo chlorophyll fluorescence study. J Exp Bot 167:709–716

    CAS  Google Scholar 

  • Tian Y, Sacharz J, Ware MA, Zhang H, Ruban AV (2017) Effects of periodic photoinhibitory light exposure on physiology and productivity of Arabidopsis plants grown under low light. J Exp Bot 68:4249–4262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Jiang L, Li Y, Chen Q, Ye Y, Zhang Y, Luo Y, Sun B, Wang X, Tang H (2018) Effect of red and blue light on anthocyanin accumulation and differential gene expression in strawberry (Fragaria x anaassa). Molecules 234:820. https://doi.org/10.3390/molecules23040820

    Article  CAS  Google Scholar 

  • Zhu XG, 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 55:1167–1175

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Strategic Priority Research Program of the Chinese Academy of Sciences, Grant No. XDB27020105, CAS-TWAS President’s Fellowship Program, the Chinese Academy of Sciences (CAS) strategic leading project on agriculture XDA08020301 and National Basic Research and Development Program of the Ministry of Science and Technology of China 2015CB150104, 2014AA101601, National Science Foundation # C020401. Govindjee thanks the office of Information Technology, Life Sciences, the Department of Plant Biology and the Department of Biochemistry for support.

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SH and XZ designed and conducted the research. SH, NK, SP, MQ, and JJ performed research. SH, NK, G, and XZ wrote the manuscript.

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Correspondence to Xin-Guang Zhu.

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Hamdani, S., Khan, N., Perveen, S. et al. Changes in the photosynthesis properties and photoprotection capacity in rice (Oryza sativa) grown under red, blue, or white light. Photosynth Res 139, 107–121 (2019). https://doi.org/10.1007/s11120-018-0589-6

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