Environmental Science and Pollution Research

, Volume 24, Issue 2, pp 1380–1388 | Cite as

Fe deficiency induced changes in rice (Oryza sativa L.) thylakoids

  • Yuwen Wang
  • Chao Xu
  • Kang Li
  • Xiaojie Cai
  • Min Wu
  • Guoxiang ChenEmail author
Research Article


Iron deficiency is an important abiotic stress that limits productivity of crops all over the world. We selected a hybrid rice (Oryza sativa L.), LYPJ, which is super high-yield and widely cultured in China, to investigate changes in the components and structure of thylakoid membranes and photosynthetic performance in response to iron deficiency. Our results demonstrated that photosystem I (PSI) is the primary target for iron deficiency, while the changes in photosystem II (PSII) are important for rebuilding a balance in disrupted energy utilization and dissipation caused by differential degradation of photosynthetic components. The result of immunoblot analysis suggested that the core subunit PsaA declined drastically, while PsbA remained relatively stable. Furthermore, several organizational changes of the photosynthetic apparatus were found by BN-PAGE, including a marked decrease in the PSI core complexes, the Cytb 6 /f complex, and the trimeric form of the LHCII antenna, consistent with the observed unstacking grana. The fluorescence induction analysis indicated a descending PSII activity with energy dissipation enhanced markedly. In addition, we proposed that the crippled CO2 assimilation could be compensated by the enhanced of phosphoenolpyruvate carboxylase (PEPC), which is suggested by the decreased ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) and photosynthetic efficiency.


Thylakoid complexes Photosynthetic apparatus Rice Fe deficiency 



Blue native






Light harvesting complex


Polyacrylamide gel electrophoresis


Phosphoenolpyruvate carboxylase


Photosystem I


Photosystem II


Sodium dodecyl sulfate


Ribulose-1,5-bisphosphate carboxylase/oxygenase



This research was supported by the National Natural Science Foundation of China (No. 31271621), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and NSFC for Talents Training in Basic Science (J1103507, J1210025).

Authors’ contribution

This work was designed by G. Chen. Data analysis was performed by Y. Wang and M. Wu. Experiments were performed by K. Li and X. Cai. Y. Wang and C. Xu wrote the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abadía J, Morales F, Abadía A (1999) Photosystem II efficiency in low chlorophyll, iron-deficient leaves. Plant Soil 215:183–192CrossRefGoogle Scholar
  2. Andaluz S, López-Millán AF, De las Rivas J, Aro EM, Abadía J, Abadía A (2006) Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth Res 89:141–155CrossRefGoogle Scholar
  3. Andersson B, Aro EM (2001) Photodamage and D1 protein turnover in photosystem II. In: Aro EM, Andersson B (eds) Regulation of photosynthesis. Kluwer Academic Publishers, Dordrecht, pp. 377–393Google Scholar
  4. Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphenoloxidase in Bete vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  5. Basa B, Lattanzio G, Solti Á, Tóth B, Abadía J, Fodor F, Sárvári É (2014) Changes induced by cadmium stress and iron deficiency in the composition and organization of thylakoid complexes in sugar beet (Beta vulgaris L.). Environ Exp Bot 101:1–11CrossRefGoogle Scholar
  6. Bertamini M, Muthuchelian K, Nedunchezhian N (2002) Iron deficiency induced changes on the donor side of PSII in field grown grapevine (Vitis vinifera L. cv. Pinot noir) leaves. Plant Sci 162:599–605CrossRefGoogle Scholar
  7. Bertamini M, Nedunchezhian N, Borghi B (2001) Effect of iron deficiency induced changes on photosynthetic pigments, ribulose-1, 5-bisphosphate carboxylase, and photosystem activities in field grown grapevine (Vitis vinifera L. cv. Pinot noir) leaves. Photosynthetica 39:59–65CrossRefGoogle Scholar
  8. Chen L, Ding C, Zhao X, Xu J, Mohammad AA, Wang S, Ding Y (2015) Differential regulation of proteins in rice (Oryza sativa L.) under iron deficiency. Plant Cell Rep 34:83–96CrossRefGoogle Scholar
  9. Chen Y, Barak P (1982) Iron nutrition of plants in calcareous soils. Adv Agron 35:240Google Scholar
  10. Choquet Y, Vallon O (2000) Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 82:615–634CrossRefGoogle Scholar
  11. Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583CrossRefGoogle Scholar
  12. Eggink LL, LoBrutto R, Brune DC, Brusslan J, Yamasato A, Tanaka A, Hoober JK (2004) Synthesis of chlorophyll b: localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit. BMC Plant Biol 4:5CrossRefGoogle Scholar
  13. Garab G, Cseh Z, Kovács L, Rajagopal S, Várkonyi Z, Wentworth M, Mustárdy L, Dér A, Ruban AV, Papp E, Holzenburg A, Horton P (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41:15121–15129CrossRefGoogle Scholar
  14. Guha A, Sengupta D, Reddy AR (2013) Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J Photoch Photobio B 119:71–83CrossRefGoogle Scholar
  15. Hoagland DR, Arnon DI (1938) The water-culture method for growing plants without soil. Calif Agri Ext Publ 347:35–47Google Scholar
  16. Jelali N, Salah IB, M’sehli W, Donnini S, Zocchi G, Gharsalli M (2011) Comparison of three pea cultivars (Pisum sativum) regarding their responses to direct and bicarbonate-induced iron deficiency. Sci Hortic 129:548–553CrossRefGoogle Scholar
  17. Jiang CD, Gao HY, Zou Q, Shi L (2007) Effects of iron deficiency on photosynthesis and photosystem II function in soybean leaf. J Plant Physiol Mol Bio 1:53–60Google Scholar
  18. Jin MX, Mi HL, Ye JY, Shen YG (2000) Mathematical analysis of post-illumination transient increase in chlorophyll fluorescence and its dependence upon illumination duration in maize leaves. Acta Phytophysiol Sin 26:219–226Google Scholar
  19. Joaquín-Ramos A, Huerta-Ocampo JÁ, Barrera-Pacheco A, De León-Rodríguez A, Baginsky S, de la Rosa APB (2014) Comparative proteomic analysis of amaranth mesophyll and bundle sheath chloroplasts and their adaptation to salt stress. J Plant Physiol 171:1423–1435CrossRefGoogle Scholar
  20. Ke Y, Han G, He H, Li J (2009) Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochem Biophys Res Commun 379:133–138CrossRefGoogle Scholar
  21. Kirchhoff H (2008) Molecular crowding and order in photosynthetic membranes. Trends Plant Sci 13:201–207CrossRefGoogle Scholar
  22. Kornyeyev D, Hendrickson L (2007) Energy partitioning in photosystem II complexes subjected to photoinhibitory treatment. Funct Plant Biol 34:214–220CrossRefGoogle Scholar
  23. Kügler M, Jänsch L, Kruft V, Schmitz UK, Braun HP (1997) Analysis of the chloroplast protein complexes by blue-native polyacrylamide gel electrophoresis (BN-PAGE). Photosynth Res 53:35–44CrossRefGoogle Scholar
  24. Ladygin VG (2004) Changes in the biochemical composition, structure, and function of pea leaf chloroplasts in iron deficiency and root anoxia. Appl Biochem Microbiol 40:506–516CrossRefGoogle Scholar
  25. Laganowsky A, Gómez SM, Whitelegge JP, Nishio JN (2009) Hydroponics on a chip: analysis of the Fe deficient Arabidopsis thylakoid membrane proteome. J Proteome 72:397–415CrossRefGoogle Scholar
  26. Morales F, Moise N, Quílez R, Abadía A, Abadía J, Moya I (2001) Iron deficiency interrupts energy transfer from a disconnected part of the antenna to the rest of photosystem II. Photosynth Res 70:207–220CrossRefGoogle Scholar
  27. Mori S, Nishizawa N, Hayashi H, Chino M, Yoshimura E, Ishihara J (1991) Why are young rice plants highly susceptible to iron deficiency? Plant Soil 130:143–156CrossRefGoogle Scholar
  28. Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21:6709–6720CrossRefGoogle Scholar
  29. Msilini N, Essemine J, Zaghdoudi M, Harnois J, Lachaâl M, Ouerghi Z, Carpentier R (2013) How does iron deficiency disrupt the electron flow in photosystem I of lettuce leaves? J Plant Physiol 170:1400–1406CrossRefGoogle Scholar
  30. Msilini N, Zaghdoudi M, Govindachary S, Lachaâl M, Ouerghi Z, Carpentier R (2011) Inhibition of photosynthetic oxygen evolution and electron transfer from the quinone acceptor QA to QB by iron deficiency. Photosynth Res 107:247–256CrossRefGoogle Scholar
  31. Muneer S, Lee BR, Kim KY, Park SH, Zhang Q, Kim TH (2014) Involvement of sulphur nutrition in modulating iron deficiency responses in photosynthetic organelles of oilseed rape (Brassica napus L.). Photosynth Res 119:319–329CrossRefGoogle Scholar
  32. Nenova VR (2009) Growth and photosynthesis of pea plants under different iron supply. Acta Physiol Plant 31:385–391CrossRefGoogle Scholar
  33. Osório J, Osório ML, Correia PJ, Varennes AD, Pestana M (2014) Chlorophyll fluorescence imaging as a tool to understand the impact of iron deficiency and resupply on photosynthetic performance of strawberry plants. Sci Horti 165:148–155CrossRefGoogle Scholar
  34. Peguero-Pina JJ, Gil-Pelegrín E, Morales F (2013) Three pools of zeaxanthin in Quercus coccifera leaves during light transitions with different roles in rapidly reversible photoprotective energy dissipation and photoprotection. J Exp Bot 64:1649–1661CrossRefGoogle Scholar
  35. Qureshi MI, D’Amici GM, Fagioni M, Rinalducci S, Zolla L (2010) Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. J Plant Physiol 167:761–770CrossRefGoogle Scholar
  36. Saito A, Shimizu M, Nakamura H, Maeno S, Katase R, Miwa E, Higuchi K, Sonoike K (2014) Fe deficiency induces phosphorylation and translocation of Lhcb1 in barley thylakoid membranes. FEBS Lett 588:2042–2048CrossRefGoogle Scholar
  37. Shao J, Zhang Y, Yu J, Guo L, Ding Y (2011) Isolation of thylakoid membrane complexes from rice by a new double-strips BN/SDS-PAGE and bioinformatics prediction of stromal ridge subunits interaction. PLoS One 6:e20342CrossRefGoogle Scholar
  38. Sharma S (2007) Adaptation of photosynthesis under iron deficiency in maize. J Plant Physiol 164:1261–1267CrossRefGoogle Scholar
  39. Sharma S, Sanwal GG (1992) Effect of Fe-deficiency on the photosynthetic system of maize. J Plant Physiol 140:527–530CrossRefGoogle Scholar
  40. Strasserf RJ, Srivastava A (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42CrossRefGoogle Scholar
  41. Terry N, Abadía J (1986) Function of iron in chloroplasts. J Plant Nutr 9:609–646CrossRefGoogle Scholar
  42. Thoiron S, Pascal N, Briat JF (1997) Impact of iron deficiency and iron re-supply during the early stages of vegetative development in maize (Zea mays L.). Plant Cell Environ 20:1051–1060CrossRefGoogle Scholar
  43. Timperio AM, D’Amici GM, Barta C, Loreto F, Zolla L (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J Exp Bot 58:3695–3710CrossRefGoogle Scholar
  44. Winder TL, Nishio JN (1995) Early iron deficiency stress response in leaves of sugar beet. Plant Physiol 108:1487–1494CrossRefGoogle Scholar
  45. Yadavalli V, Neelam S, Rao AS, Reddy AR, Subramanyam R (2012) Differential degradation of photosystem I subunits under iron deficiency in rice. J Plant Physiol 169:753–759CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Yuwen Wang
    • 1
  • Chao Xu
    • 1
  • Kang Li
    • 1
  • Xiaojie Cai
    • 1
  • Min Wu
    • 1
    • 2
  • Guoxiang Chen
    • 1
    Email author
  1. 1.Jiangsu Key Laboratory of Biodiversity and Biotechnology, Life Sciences CollegeNanjing Normal UniversityNanjingChina
  2. 2.Zijin CollegeNanjing University of Science and TechnologyNanjingChina

Personalised recommendations