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Photoprotection and growth under different lights of Arabidopsis single and double mutants for energy dissipation (npq4) and state transitions (pph1)

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Arabidopsis single and double mutants for energy dissipation (npq4) and state transitions (pph1, blocked in State II) show enhanced growth and flowers + siliques production under controlled low-light conditions.

Abstract

Non-photochemical quenching (NPQ) is a short-term regulation important to maintain efficient photosynthesis and to avoid photooxidative damages by dissipation of excess energy. Full activation of NPQ in plants requires the protonation of the PsbS protein, which is the sensor of the low lumenal pH triggering the thermal dissipation. State transitions are a second important photosynthetic regulation to respond to changes in light quality and unbalanced excitation of photosystems. State transitions allow energy redistribution between PSI and PSII through the reversible exchange of LHCII antenna complexes between photosystems thanks to the opposite action of the STN7 kinase and PPH1 phosphatase: phosphorylation of LHCII promotes its mobilization from PSII to PSI, while dephosphorylation has the opposite effect. In this work, we produced the pph1/npq4 double mutant and characterized some photosynthetic, growth and reproduction properties in comparison with wild-type and single-mutant plants in high- and low-light conditions. Results indicate that in high light, the pph1 mutant maintains good photoprotection ability, while npq4 plants show more susceptibility to photodamages. The pph1/npq4 double mutant showed a resistance to high-light stress similar to that of the single npq4 mutant. In low-light condition, the single mutants showed a significant increase of growth and flowering compared to wild-type plants and this effect was further enhanced in the pph1/npq4 double mutant. Results suggest that photosynthetic optimisation to improve crop growth and productivity might be possible, at least under controlled low-light conditions, by modifying NPQ and regulation of state transitions.

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References

  • Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

    Article  CAS  PubMed  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    Article  CAS  PubMed  Google Scholar 

  • Allen JF (2003) Botany. State transitions–a question of balance. Science 299:1530–1532

    Article  CAS  PubMed  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Asada K (2002) The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  Google Scholar 

  • Awan SF, Khan IA, Khan AA, Schneider A, Altaf A, Ahmad R, Leister D (2008) Screening of Arabidopsis mutant for functional genomic studies. Pak J Bot 40:2071–2080

    CAS  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  CAS  PubMed  Google Scholar 

  • Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall’osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284:15255–15266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383

    Article  CAS  PubMed  Google Scholar 

  • Bonente G, Howes BD, Caffarri S, Smulevich G, Bassi R (2008) Interactions between the photosystem II subunit PsbS and xanthophylls studied in vivo and in vitro. J Biol Chem 283:8434–8445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011) Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campoli C, Caffarri S, Svensson JT, Bassi R, Stanca AM, Cattivelli L, Crosatti C (2009) Parallel pigment and transcriptomic analysis of four barley albina and xantha mutants reveals the complex network of the chloroplast-dependent metabolism. Plant Mol Biol 71:173–191

    Article  CAS  PubMed  Google Scholar 

  • Crepin A, Caffarri S (2015) The specific localizations of phosphorylated Lhcb1 and Lhcb2 isoforms reveal the role of Lhcb2 in the formation of the PSI-LHCII supercomplex in Arabidopsis during state transitions. Biochim Biophys Acta Bioenerg 1847:1539–1548

    Article  CAS  Google Scholar 

  • Croce R, Canino g, Ros F, Bassi R (2002) Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41:7334–7343

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  CAS  PubMed  Google Scholar 

  • Dominici P, Caffarri S, Armenante F, Ceoldo S, Crimi M, Bassi R (2002) Biochemical properties of the PsbS subunit of photosystem II either purified from chloroplast or recombinant. J Biol Chem 277:22750–22758

    Article  CAS  PubMed  Google Scholar 

  • Dong L, Tu W, Liu K, Sun R, Liu C, Wang K, Yang C (2015) The PsbS protein plays important roles in photosystem II supercomplex remodeling under elevated light conditions. J Plant Physiol 172:33–41

    Article  CAS  PubMed  Google Scholar 

  • Funk C, Adamska I, Green BR, Andersson B, Renger G (1995) The nuclear-encoded chlorophyll-binding photosystem II-S protein is stable in the absence of pigments. J Biol Chem 270:30141–30147

    Article  CAS  PubMed  Google Scholar 

  • Galka P, Santabarbara S, Khuong TTH, Degand H, Morsomme P, Jennings RC, Boekema EJ, Caffarri S (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24:2963–2978

    Article  CAS  PubMed  PubMed Central  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 

  • Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932

    Article  CAS  PubMed  Google Scholar 

  • Gerotto C, Alboresi A, Meneghesso A, Jokel M, Suorsa M, Aro EM, Morosinotto T (2016) Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proc Natl Acad Sci USA 113:12322–12327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmore AM, Yamamoto HY (1992) Dark induction of zeaxanthin-dependent nonphotochemical fluorescence quenching mediated by ATP. Proc Natl Acad Sci USA 89:1899–1903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Głowacka K, Kromdijk J, Kucera K, Xie J, Cavanagh AP, Leonelli L, Leakey ADB, Ort DR, Niyogi KK, Long SP (2018) Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop. Nature Communications 9:868. https://doi.org/10.1038/s41467-018-03231-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golan T, Muller-Moule P, Niyogi KK (2006) Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants. Plant Cell Environ 29:879–887

    Article  CAS  PubMed  Google Scholar 

  • Gorbunov MY, Kuzminov FI, Fadeev VV, Kim JD, Falkowski PG (2011) A kinetic model of non-photochemical quenching in cyanobacteria. Biochim Biophys Acta Bioenerg 1807:1591–1599

    Article  CAS  Google Scholar 

  • Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305

    Article  CAS  PubMed  Google Scholar 

  • Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holzwarth AR, Miloslavina Y, Nilkensb M, Jahnsb P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262–267

    Article  CAS  Google Scholar 

  • Horton P, Ruban AV (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56:365–373

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579:4201–4206

    Article  CAS  PubMed  Google Scholar 

  • Hubbart S, Ajigboye OO, Horton P, Murchie EH (2012) The photoprotective protein PsbS exerts control over CO(2) assimilation rate in fluctuating light in rice. Plant J 71:402–412

    CAS  PubMed  Google Scholar 

  • Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283–289

    Article  CAS  PubMed  Google Scholar 

  • Johnson MP, Ruban AV (2011) Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced DeltapH. J Biol Chem 286:19973–19981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalituho L, Grasses T, Graf M, Rech J, Jahns P (2006) Characterization of a nonphotochemical quenching-deficient Arabidopsis mutant possessing an intact PsbS protein, xanthophyll cycle and lumen acidification. Planta 223:532–541

    Article  CAS  PubMed  Google Scholar 

  • Kasajima I, Ebana K, Yamamoto T, Takahara K, Yano M, Kawai-Yamada M, Uchimiya H (2011) Molecular distinction in genetic regulation of nonphotochemical quenching in rice. Proc Natl Acad Sci USA 108:13835–13840

    Article  PubMed  PubMed Central  Google Scholar 

  • Kereiche S, Kiss AZ, Kouril R, Boekema EJ, Horton P (2010) The PsbS protein controls the macro-organisation of photosystem II complexes in the grana membranes of higher plant chloroplasts. FEBS Lett 584:759–764

    Article  CAS  PubMed  Google Scholar 

  • Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978

    Article  CAS  PubMed  Google Scholar 

  • Krah NM, Logan BA (2010) Loss of psbS expression reduces vegetative growth, reproductive output, and light-limited, but not light-saturated, photosynthesis in Arabidopsis thaliana (Brassicaceae) grown in temperate light environments. Am J Bot 97:644–649

    Article  CAS  PubMed  Google Scholar 

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    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 

  • Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  PubMed  Google Scholar 

  • Lemeille S, Willig A, Depege-Fargeix N, Delessert C, Bassi R, Rochaix JD (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7:e45

    Article  CAS  PubMed  Google Scholar 

  • Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  CAS  PubMed  Google Scholar 

  • Li X, Phippard A, Pasari J, Niyogi K (2002a) Structural-functional analysis of Photosystem II subunit S (PsbS) in vivo. Funct Plant Biol 29:1131–1139

    Article  PubMed  Google Scholar 

  • Li XP, Muller-Moule P, Gilmore AM, Niyogi KK (2002b) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci U S A 99:15222–15227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • Mao HB, Li GF, Ruan X, Wu QY, Gong YD, Zhang XF, Zhao NM (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b6f complex in Synechocystis sp. PCC 6803. FEBS Lett 519:82–86

    Article  CAS  PubMed  Google Scholar 

  • Mekala NR, Suorsa M, Rantala M, Tikkanen M, Aro EM (2015) Plants actively avoid state transitions upon changes in light intensity: role of light-harvesting complex II protein dephosphorylation in high light. Plant Physiol 168:721–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage ? Trends Plant Sci 4:130–135

    Article  CAS  PubMed  Google Scholar 

  • Minagawa J (2011) State transitions–the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim Biophys Acta Bioenerg 1807:897–905

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  CAS  PubMed  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251

    Article  CAS  PubMed  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  CAS  PubMed  Google Scholar 

  • Niyogi K, Truong T (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382

    Article  CAS  PubMed  Google Scholar 

  • Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. Plos Biology 8:e1000288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puthiyaveetil S, Ibrahim IM, Allen JF (2012) Oxidation-reduction signalling components in regulatory pathways of state transitions and photosystem stoichiometry adjustment in chloroplasts. Plant Cell Environ 35:347–359

    Article  CAS  PubMed  Google Scholar 

  • Rintamaki E, Salonen M, Suoranta UM, Carlberg I, Andersson B, Aro EM (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem 272:30476–30482

    Article  CAS  PubMed  Google Scholar 

  • Rintamaki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV (2017) Quantifying the efficiency of photoprotection. Philos Trans R Soc Lond B Biol Sci 372

  • Ruban AV, Murchie EH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim Biophys Acta Bioenerg 1817:977–982

    Article  CAS  Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CD (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta Bioenerg 1817:167–181

    Article  CAS  Google Scholar 

  • Sacharz J, Giovagnetti V, Ungerer P, Mastroianni GV, Ruban AV (2017) The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching. Nature Plants 3. https://doi.org/10.1038/nplants.2016.225

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA 107:4782–4787

    Article  PubMed  PubMed Central  Google Scholar 

  • Shikanai T, Yamamoto H (2017) Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts. Mol Plant 10:20–29

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235–238

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M, Grieco M, Jarvi S, Tikkanen M, Jansson S, Aro EM, Pietrzykowska M, Paakkarinen V, Nurmi M, Rantala M, Kangasjarvi S (2012) PRoton gradient regulation5 is essential for proper acclimation of arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sylak-Glassman EJ, Malnoe A, De Re E, Brooks MD, Fischer AL, Niyogi KK, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tibiletti T, Auroy P, Peltier G, Caffarri S (2016) Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol 171:2717–2730

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tikkanen M, Nurmi M, Kangasjarvi S, Aro EM (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta Bioenerg 1777:1432–1437

    Article  CAS  Google Scholar 

  • Tikkanen M, Grieco M, Kangasjarvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tjus SE, Møller BL, Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116:755–764

    Article  CAS  PubMed  Google Scholar 

  • Veeranjaneyulu K, Leblanc RM (1994) Action spectra of photosystems I and II in state 1 and state 2 in intact sugar maple leaves. Plant Physiol 104:1209–1214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilhelm C, Selmar D (2011) Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis. J Plant Physiol 168:79–87

    Article  CAS  PubMed  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. Embo J 20:3623–3630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the French National Research Agency Grant ANR-2012-JCJC-0001-01, the 322 project of the Vietnamese Government and the project of Vietnam University of Forestry, 2014. Bernard Genty (BIAM, Biosciences and Biotechnologies Institute of Aix-Marseille – AMU/CRNS/CEA) is thanked for helpful discussion.

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  1. Aix Marseille Université, CEA, CNRS, Biosciences and Biotechnologies Institute of Aix-Marseille (BIAM), Equipe de Luminy de Génétique et Biophysique des Plantes, 13009, Marseille, France

    Thi Thu Huong Khuong, Christophe Robaglia & Stefano Caffarri

  2. Cell Technology Laboratory-CFB, Vietnam National University of Forestry, Hanoi, Vietnam

    Thi Thu Huong Khuong

  3. The Key Laboratory of Enzyme and Protein Technology (KLEPT), Hanoi University of Science (HUS), Vietnam National University in Hanoi (VNU), Hanoi, Vietnam

    Thi Thu Huong Khuong

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Khuong, T.T.H., Robaglia, C. & Caffarri, S. Photoprotection and growth under different lights of Arabidopsis single and double mutants for energy dissipation (npq4) and state transitions (pph1). Plant Cell Rep 38, 741–753 (2019). https://doi.org/10.1007/s00299-019-02403-3

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