Photosynthesis Research

, Volume 125, Issue 1–2, pp 151–166 | Cite as

Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines

  • Marian Brestic
  • Marek Zivcak
  • Kristyna Kunderlikova
  • Oksana Sytar
  • Hongbo Shao
  • Hazem M. Kalaji
  • Suleyman I. Allakhverdiev
Regular Paper


In vivo analyses of electron and proton transport-related processes as well as photoprotective responses were carried out at different stages of growth in chlorophyll b (Chl b)-deficient mutant lines (ANK-32A and ANK-32B) and wild type (WT) of wheat (Triticum aestivum L.). In addition to a high Chl ab ratio, ANK mutants had a lower content of photo-oxidizable photosystem I (PSI, P m), and several parameters indicated a low PSI/PSII ratio. Moreover, simultaneous measurements of Chl fluorescence and P700 indicated a shift of balance between redox poise of the PSII acceptor side and the PSII donor side, with preferential reduction of the plastoquinone pool, resulting in an over reduced PSI acceptor side (high Φ NA values). This was the probable reason for PSI inactivation observed in the ANK mutants, but not in WT. In later growth phases, we observed partial relief of “chlorina symptoms,” toward WT. Measurements of ΔA 520 decay confirmed that, in early growth stages, the ANK mutants with low PSI content had a limited capacity to build up the transthylakoid proton gradient (ΔpH) needed to trigger non-photochemical quenching (NPQ) and to regulate the electron transport by cytochrome b 6/f. Later, the increase in the PSI/PSII ratio enabled ANK mutants to reach full NPQ, but neither over reduction of the PSI acceptor side nor PSI photoinactivation due to imbalance between the activity of PSII and PSI was mitigated. Thus, our results support the crucial role of proper regulation of linear electron transport in the protection of PSI against photoinhibition. Moreover, the ANK mutants of wheat showing the dynamic developmental changes in the PSI/PSII ratio are presented here as very useful models for further studies.


Chlorina mutants Wheat Non-photochemical quenching Chlorophyll fluorescence Transthylakoid proton gradient PSI photoinhibition 


See Materials and methods section for other symbols representing chlorophyll fluorescence and P700 parameters

\(A_{{{\text{CO}}_{2} }}\)

CO2 assimilation rate




Chlorophyll a fluorescence

Cyt b6/f

Cytochrome b 6/f


Electrochromic bandshift


Light emitting diode


Light harvesting complex


Primary electron donor of PSI (reduced form)


Primary electron donor of PSI (oxidized form)


Photosynthetic active radiation


Proton motive force




Photosystem I


Photosystem II


Primary, secondary PSII acceptor


Reaction centers


Reactive oxygen species


pH-dependent energy dissipation


Wild type; the genotype with normal chlorophyll synthesis


Absorbance changes at 520 nm


Transthylakoid pH gradient



This work was supported by the European Community under the Project No. 26220220180: “Construction of the ‘AgroBioTech’ Research Centre.” SIA was supported by Grants from the Russian Foundation for Basic Research, and by Molecular and Cell Biology Programs of the Russian Academy of Sciences.


  1. Agati G, Mazzinghi P, Fusi F, Ambrosini I (1995) The F685F730 chlorophyll fluorescence ratio as a tool in plant physiology: response to physiological and environmental factors. J Plant Physiol 145:228–238CrossRefGoogle Scholar
  2. Agati G, Mazzinghi P, Lipucci di Paola M, Cecchi G, Fusi F (1996) The F685/F730 chlorophyll fluorescence ratio as indicator of chilling stress in plants. J Plant Physiol 148:384–390CrossRefGoogle Scholar
  3. Andrews JR, Fryer MJ, Baker NR (1995) Consequences of LHC II deficiency for photosynthetic regulation in chlorina mutants of barley. Photosynth Res 44:81–91PubMedCrossRefGoogle Scholar
  4. Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol 50:601–639CrossRefGoogle Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113PubMedCrossRefGoogle Scholar
  6. Bossmann B, Knoetzel J, Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth Res 52:127–136CrossRefGoogle Scholar
  7. Brestic M, Zivcak M, Olsovska K, Repkova J (2008) Functional study of PS II and PS I energy use and dissipation mechanisms in barley wild type and chlorina mutants under high light conditions. In: Photosynthesis. Energy from the sun. Springer, Dordrecht, pp 1407–1411Google Scholar
  8. Brestic M, Zivcak M, Olsovska K, Shao HB, Kalaji HM, Allakhverdiev SI (2014) Reduced glutamine synthetase activity plays a role in control of photosynthetic responses to high light in barley leaves. Plant Physiol Biochem 81:74–83PubMedCrossRefGoogle Scholar
  9. Briantais JM, Vernotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138PubMedCrossRefGoogle Scholar
  10. Bukhov N, Carpentier R (2004) Alternative photosystem I-driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33PubMedCrossRefGoogle Scholar
  11. Cruz JA, Avenson TJ, Kanazawa A, Takizawa K, Edwards GE, Kramer DM (2005) Plasticity in light reactions of photosynthesis for energy production and photoprotection. J Exp Bot 56:395–406PubMedCrossRefGoogle Scholar
  12. Demmig-Adams B (1990) Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24CrossRefGoogle Scholar
  13. Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. N Phytol 172:11–21CrossRefGoogle Scholar
  14. Dinç E, Ceppi MG, Tóth SZ, Bottka S, Schansker G (2012) The chl a fluorescence intensity is remarkably insensitive to changes in the chlorophyll content of the leaf as long as the chl a/b ratio remains unaffected. Biochim Biophys Acta 1817:770–779PubMedCrossRefGoogle Scholar
  15. Eullaffroy P, Vernet G (2003) The F684/F735 chlorophyll fluorescence ratio: a potential tool for rapid detection and determination of herbicide phytotoxicity in algae. Water Res 37:1983–1990PubMedCrossRefGoogle Scholar
  16. Falbel TG, Staehelin LA (1994) Characterization of a family of chlorophyll-deficient wheat and barley mutants with defects in the Mg-insertion step of chlorophyll biosynthesis. Plant Physiol 104:639–648PubMedCentralPubMedCrossRefGoogle Scholar
  17. Falbel TG, Staehelin LA (1996) Partial blocks in the early steps of the chlorophyll synthesis pathway: a common feature of chlorophyll b-deficient mutants. Physiol Plant 97:311–320CrossRefGoogle Scholar
  18. Falbel TG, Meehl JB, Staehelin LA (1996) Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiol 112:821–832PubMedCentralPubMedCrossRefGoogle Scholar
  19. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661PubMedCrossRefGoogle Scholar
  20. Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence of intact leaves at room temperature. Biochim Biophys Acta 1556:239–246PubMedCrossRefGoogle Scholar
  21. Georgieva K, Fedina I, Maslenkova L, Peeva V (2003) Response of chlorina barley mutants to heat stress under low and high light. Funct Plant Biol 30:515–524CrossRefGoogle Scholar
  22. Ghirardi ML, Melis A (1988) Chlorophyll b deficiency in soybean mutants. I. Effects on photosystem stoichiometry and chlorophyll antenna size. Biochim Biophys Acta 932:130–137CrossRefGoogle Scholar
  23. Ghozlen NB, Cerovic ZG, Germain C, Latouche G, Toutain S (2010) Non-destructive optical monitoring of grape maturation by proximal sensing. Sensors 10:10040–10068PubMedCentralPubMedCrossRefGoogle Scholar
  24. Gilmore AM, Hazlett TL, Debrunner PG (1996) Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynth Res 48:171–187PubMedCrossRefGoogle Scholar
  25. Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114PubMedCrossRefGoogle Scholar
  26. Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji MH, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakhverdiev SI, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490–1498PubMedCrossRefGoogle Scholar
  27. Graan T, Ort DR (1986) Detection of oxygen-evolving photosystem II centers inactive in plastoquinone reduction. Biochim Biophys Acta 852:320–330CrossRefGoogle Scholar
  28. Grieco M, Tikkanen M, Paakkarinen V, Kangasjärvi S, Aro EM (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves Photosystem I under fluctuating white light. Plant Physiol 160:1896–1910PubMedCentralPubMedCrossRefGoogle Scholar
  29. Harrison MA, Nemson JA, Melis A (1993) Assembly and composition of the chlorophyll ab light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll bless and chlorophyll b-deficient mutants. Photosynth Res 38:141–151PubMedCrossRefGoogle Scholar
  30. Ivanov AG, Krol M, Zeinalov Y, Huner NPA, Sane PV (2008) The lack of LHCII proteins modulates excitation energy partitioning and PSII charge recombination in Chlorina F2 mutant of barley. Physiol Mol Biol Plants 14:205–215PubMedCentralPubMedCrossRefGoogle Scholar
  31. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389PubMedCrossRefGoogle Scholar
  32. Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322PubMedCentralPubMedCrossRefGoogle Scholar
  33. Joliot P, Joliot A (2002) Cyclic electron transfer in plant leaf. Proc Natl Acad Sci USA 99:10209–10214PubMedCentralPubMedCrossRefGoogle Scholar
  34. Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158PubMedCentralPubMedCrossRefGoogle Scholar
  35. Klughammer C, Schreiber U (1994) Saturation pulse method for assessment of energy conversion in PS I. Planta 192:261–268CrossRefGoogle Scholar
  36. Kohzuma K, Cruz JA, Akashi K, Munekage YN, Hoshiyasu S, Kramer DM, Yokota A (2009) The long-term responses of the photosynthetic proton circuit to drought. Plant, Cell Environ 32:209–219CrossRefGoogle Scholar
  37. 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 55:990–1004PubMedCrossRefGoogle Scholar
  38. Kosuge K, Watanabe N, Kuboyama T (2011) Comparative genetic mapping of the chlorina mutant genes in genus Triticum. Euphytica 179:257–263CrossRefGoogle Scholar
  39. Koval SF (1997) The catalogue of near-isogenic lines of Novosibirskaya 67 common wheat and principles of their use in experiments. Russ J Genet 33:995–1000Google Scholar
  40. Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32PubMedCrossRefGoogle Scholar
  42. Kramer DM, Johnson G, Edwards GE, Kiirats O (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218PubMedCrossRefGoogle Scholar
  43. Kreslavski VD, Lankin AV, Vasilyeva GK, Luybimov VY, Semenova GN, Schmitt F-J, Friedrich T, Allakhverdiev SI (2014) Effects of polyaromatic hydrocarbons on photosystem II activity in pea leaves. Plant Physiol Biochem 81:135–142PubMedCrossRefGoogle Scholar
  44. Krol M, Spangfort MD, Huner NP, Oquist G, Gustafsson P, Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107:873–883PubMedCentralPubMedCrossRefGoogle Scholar
  45. Laisk A, Talts E, Oja V, Eichelmann H, Peterson RB (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95PubMedCrossRefGoogle Scholar
  46. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395PubMedCrossRefGoogle Scholar
  47. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260PubMedCrossRefGoogle Scholar
  48. Lichtenthaler HL (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Method Enzymol 148:350–382Google Scholar
  49. Lichtenthaler HK, Hak R, Rinderle U (1990) The chlorophyll fluorescence ratio F690/F730 in leaves of different chlorophyll content. Photosynth Res 25:295–298PubMedCrossRefGoogle Scholar
  50. Lin ZF, Peng CL, Lin GZ, Ou ZY, Yang CW, Zhang JL (2003) Photosynthetic characteristics of two new chlorophyll b-less rice mutants. Photosynthetica 41:61–67CrossRefGoogle Scholar
  51. Mathur S, Allakhverdiev SI, Jajoo A (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochim Biophys Acta 1807:22–29PubMedCrossRefGoogle Scholar
  52. Melis A (1995) Functional properties of PS IIβ in spinach chloroplasts. Biochim Biophys Acta 808:334–342CrossRefGoogle Scholar
  53. Mitrofanova OP (1991) Creation of the bank of soft wheat marker genes. 1. Analysis of chlorophyll mutations. In: Koval SF (ed) Near-isogenic lines of cultivated species. ICG SO AN SSSR, Novosibirsk, pp 47–57 (in Russian)Google Scholar
  54. Miyake C (2010) Alternative electron flows (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963PubMedCrossRefGoogle Scholar
  55. Miyake C, Miyata M, Shinzaki Y, Tomizawa KI (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol 46:629–637PubMedCrossRefGoogle Scholar
  56. 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 429:579–582PubMedCrossRefGoogle Scholar
  57. Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, alpha-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133PubMedCrossRefGoogle Scholar
  58. Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460PubMedCrossRefGoogle Scholar
  59. Oukarroum A, Goltsev V, Strasser RJ (2013) Temperature effects on pea plants probed by simultaneous measurements of the kinetics of prompt fluorescence, delayed fluorescence and modulated 820 nm reflection. PLoS ONE 8:e59433PubMedCentralPubMedCrossRefGoogle Scholar
  60. Pfündel EE (1998) Estimating the contribution of photosystem I to total leaf chlorophyll fluorescence. Photosynth Res 56:185–195CrossRefGoogle Scholar
  61. Pfündel EE, Klughammer C, Meister A, Cerovic ZG (2013) Deriving fluorometer-specific values of relative PSI fluorescence intensity from quenching of F0 fluorescence in leaves of Arabidopsis thaliana and Zea mays. Photosynth Res 114:189–206PubMedCrossRefGoogle Scholar
  62. Purcell M, Carpentier R (1994) Homogeneous photobleaching of chlorophyll holochromes in a photosystem I reaction center complex. Photochem Photobiol 59:215–218CrossRefGoogle Scholar
  63. Rajagopal S, Bukhov NG, Carpentier R (2002) Changes in the structure of chlorophyll–protein complexes and excitation energy transfer during photoinhibitory treatment of isolated photosystem I submembrane particles. J Photochem Photobiol, B 62:194–200CrossRefGoogle Scholar
  64. Rajagopal S, Bukhov NG, Carpentier R (2003) Photoinhibitory light-induced changes in the composition of chlorophyll–protein complexes and photochemical activity in photosystem-I submembrane fractions. Photochem Photobiol 77:284–291PubMedCrossRefGoogle Scholar
  65. Rajagopal S, Joly D, Gauthier A, Beauregard M, Carpentier R (2005) Protective effect of active oxygen scavengers on protein degradation and photochemical function in photosystem I submembrane fractions during light stress. FEBS J 272:892–902PubMedCrossRefGoogle Scholar
  66. Rassadina VV, Averina NG, Koval SF (2005) Disturbance of chlorophyll formation at the level of 5-aminolevulinic acid and Mg-containing porphyrin synthesis in isogenic lines of spring wheat (Triticum aestivum L.) marked with genes cn-A1 and cn-D1. Dokl Biol Sci 405:472–473PubMedCrossRefGoogle Scholar
  67. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant, Cell Environ 30:1041–1051CrossRefGoogle Scholar
  68. Sacksteder CA, Kramer DM (2000) Dark-interval relaxation kinetics (DIRK) of absorbance changes as a quantitative probe of steady-state electron transfer. Photosynth Res 66:145–158PubMedCrossRefGoogle Scholar
  69. Schanker G, Strasser RJ (2005) Quantification of non-QB-reducing centers in leaves using a far-red pre-illumination. Photosynth Res 84:145–151CrossRefGoogle Scholar
  70. Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8PubMedCrossRefGoogle Scholar
  71. Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signalling in phototrophic organisms. Biochim Biophys Acta 1837:835–848PubMedCrossRefGoogle Scholar
  72. Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z Naturforsch C 43:686–698Google Scholar
  73. 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 55:1184–1193Google Scholar
  74. Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr Opin Biotechnol 26:25–30PubMedCrossRefGoogle Scholar
  75. Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247CrossRefGoogle Scholar
  76. Sonoike K (2010) Photoinhibition of photosystem I. Physiol Plant 142:56–64CrossRefGoogle Scholar
  77. Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293CrossRefGoogle Scholar
  78. Sonoike K, Kamo M, Hihara Y, Hiyama T, Enami I (1997) The mechanism of the degradation of PsaB gene product, one of the photosynthetic reaction centre subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63CrossRefGoogle Scholar
  79. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee (eds) Advances in photosynthesis and respiration: chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 321–362Google Scholar
  80. Štroch M, Čajánek M, Kalina J, Špunda V (2004) Regulation of the excitation energy utilization in the photosynthetic apparatus of chlorina f2 barley mutant grown under different irradiances. J Photochem Photobiol, B 75:41–50CrossRefGoogle Scholar
  81. Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro EM (2012) Proton gradient regulation5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948PubMedCentralPubMedCrossRefGoogle Scholar
  82. Terao T, Katoh S (1996) Antenna sizes of photosystem I and photosystem II in chlorophyll b-deficient mutants of rice. Evidence for an antenna function of photosystem II centers that are inactive in electron transport. Plant Cell Physiol 37:307–312CrossRefGoogle Scholar
  83. Terao T, Yamashita A, Katoh S (1985) Chlorophyll b-deficient mutants of rice I. Absorption and fluorescence spectra and chlorophyll a/b ratios. Plant Cell Physiol 26:1361–1367Google Scholar
  84. Terao T, Sonoike K, Yamazaki JY, Kamimura Y, Katoh S (1996) Stoichiometries of photosystem I and photosystem II in rice mutants differently deficient in chlorophyll b. Plant Cell Physiol 37:299–306CrossRefGoogle Scholar
  85. Thiele A, Winter K, Krause GH (1997) Low inactivation of D1 protein of photosystem II in young canopy leaves of Anacardium excelsum under high-light stress. J Plant Physiol 151:286–292CrossRefGoogle Scholar
  86. Tikkanen M, Grieco M, Nurmi M, Rantala M, Suorsa M, Aro EM (2012) Regulation of the photosynthetic apparatus under fluctuating growth light. Philos T R Soc B 367:3486–3493CrossRefGoogle Scholar
  87. Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215PubMedCrossRefGoogle Scholar
  88. Wang LF, Chen YY (2013) Characterization of a wide leaf mutant of rice (Oryza sativa L.) with high yield potential in field. Pak J Bot 45:921–926Google Scholar
  89. Watanabe N, Koval SF (2003) Mapping of chlorina mutant genes on the long arm of homoeologous group 7 chromosomes in common wheat with partial deletion lines. Euphytica 129:259–265CrossRefGoogle Scholar
  90. Yamazaki J (2010) Changes in the photosynthetic characteristics and photosystem stoichiometries in wild-type and Chl b-deficient mutant rice seedlings under various irradiances. Photosynthetica 48:521–529CrossRefGoogle Scholar
  91. Zivcak M, Brestic M, Balatová Z, Drevenaková P, Olsovska K, Kalaji HM, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546PubMedCrossRefGoogle Scholar
  92. Zivcak M, Brestic M, Kalaji HM, Govindjee (2014a) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354PubMedCentralPubMedCrossRefGoogle Scholar
  93. Zivcak M, Kalaji HM, Shao HB, Olšovská K, Brestič M (2014b) Photosynthetic proton and electron transport in wheat leaves under prolonged moderate drought stress. J Photochem Photobiol, B 137:107–115CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Marian Brestic
    • 1
  • Marek Zivcak
    • 1
  • Kristyna Kunderlikova
    • 1
  • Oksana Sytar
    • 1
    • 2
  • Hongbo Shao
    • 1
    • 3
  • Hazem M. Kalaji
    • 4
  • Suleyman I. Allakhverdiev
    • 5
    • 6
    • 7
  1. 1.Department of Plant PhysiologySlovak Agricultural UniversityNitraSlovak Republic
  2. 2.Department of Plant Physiology and EcologyTaras Shevchenko National University of KyivKievUkraine
  3. 3.Key Laboratory of Coastal Biology & Bioresources Utilization, Yantai Institute of Coastal Zone Research (YIC)Chinese Academy of Sciences (CAS)YantaiPeople’s Republic of China
  4. 4.Department of Plant Physiology, Faculty of Agriculture and BiologyWarsaw Agricultural University SGGWWarsawPoland
  5. 5.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  6. 6.Institute of Basic Biological ProblemsRussian Academy of SciencesMoscowRussia
  7. 7.Department of Plant Physiology, Faculty of BiologyM.V. Lomonosov Moscow State UniversityMoscowRussia

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