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Molecular Breeding

, 35:153 | Cite as

Localization of OsTLP27 in thylakoid lumen is required for accumulation of photosynthetic proteins in rice

  • ZhenHui Kang
  • JunLi Huang
  • HanYan Zou
  • GuangChao Zang
  • GuiXue Wang
Article
  • 214 Downloads

Abstract

We previously identified an AtTLP homolog, OsTLP27, in rice, whose overexpression improves chloroplast ultrastructure and photochemical efficiency. However, its molecular role in photosystem (PS) function and the related signaling pathway remain to be elucidated. In this study, using RNAi strategy, OsTLP27-RNAi transgenic plants displayed normal phenotype in medium containing sucrose, but showed growth retardation when transferred to soil under natural growth conditions. Gene expression showed that chloroplast-related genes were affected, and Western blot analysis revealed that accumulation of photosynthetic proteins was reduced significantly, indicating that OsTLP27 was important to normal PS function. Chloroplast subfraction and trypsin protection analysis showed that OsTLP27 localized in the thylakoid lumen. A yeast two-hybrid experiment revealed that OsTLP27 interacts with ribosomal protein L31 and an aldo–keto reductase (AKR) family protein. Our results suggested that OsTLP27 functions in photosynthetic protein accumulation by interacting with L31 and AKR.

Keywords

Rice Thylakoid lumen Chloroplast OsTLP27 Photosystem (PS) 

Notes

Acknowledgments

This work was supported by the National Genetically Modified Organisms Breeding Major Projects (2009ZX08009-109B), the National Natural Science Foundation of China (31271685) and the National Key Technology R&D Program of China (2011BAD35B02-05) as well as the Public Experiment Center of State Bioindustrial Base (Chongqing).

Supplementary material

11032_2015_338_MOESM1_ESM.docx (68 kb)
Supplementary material 1 (DOCX 68 kb)

References

  1. Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D (2009) A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana. Plant Cell 21(7):2036–2044PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bermudez MA, Galmes J, Moreno I, Mullineaux PM, Gotor C, Romero LC (2012) Photosynthetic adaptation to length of day is dependent on S-sulfocysteine synthase activity in the thylakoid lumen. Plant Physiol 160(1):274–288PubMedCentralPubMedCrossRefGoogle Scholar
  3. Che Y, Fu A, Hou X, McDonald K, Buchanan BB, Huang W, Luan S (2013) C-terminal processing of reaction center protein D1 is essential for the function and assembly of photosystem II in Arabidopsis. Proc Natl Acad Sci USA 110(40):16247–16252PubMedCentralPubMedCrossRefGoogle Scholar
  4. Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16(2):478–499PubMedCentralPubMedCrossRefGoogle Scholar
  5. Gupta R, Mould RM, He Z, Luan S (2002) A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proc Natl Acad Sci USA 99(24):15806–15811PubMedCentralPubMedCrossRefGoogle Scholar
  6. Hu F, Kang Z, Qiu S, Wang Y, Qin F, Yue C, Huang J, Wang G (2012) Overexpression of OsTLP27 in rice improves chloroplast function and photochemical efficiency. Plant Sci 195:125–134PubMedCrossRefGoogle Scholar
  7. Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K, Sato F (2007) Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol 145(3):668–679PubMedCentralPubMedCrossRefGoogle Scholar
  8. Jin H, Liu B, Luo L, Feng D, Wang P, Liu J, Da Q, He Y, Qi K, Wang J, Wang HB (2014) HYPERSENSITIVE TO HIGH LIGHT1 interacts with LOW QUANTUM YIELD OF PHOTOSYSTEM II1 and functions in protection of photosystem II from photodamage in Arabidopsis. Plant Cell 26(3):1213–1229PubMedCentralPubMedCrossRefGoogle Scholar
  9. Karamoko M, Cline S, Redding K, Ruiz N, Hamel PP (2012) Lumen thiol oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis. Plant Cell 23(12):4462–4475CrossRefGoogle Scholar
  10. Kieselbach T, Schroder WP (2003) The proteome of the chloroplast lumen of higher plants. Photosynth Res 78(3):249–264PubMedCrossRefGoogle Scholar
  11. Kieselbach T, Hagman Å, Andersson B, Schroder WP (1998) The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273(12):6710–6716PubMedCrossRefGoogle Scholar
  12. Kim SK, You YN, Park JC, Joung Y, Kim BG, Ahn JC, Cho HS (2011) The rice thylakoid lumenal cyclophilin OsCYP20-2 confers enhanced environmental stress tolerance in tobacco and Arabidopsis. Plant Cell Rep 31(2):417–426PubMedCrossRefGoogle Scholar
  13. Kley J, Schmidt B, Boyanov B, Stolt-Bergner PC, Kirk R, Ehrmann M, Knopf RR, Naveh L, Adam Z, Clausen T (2011) Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat Struct Mol Biol 18(6):728–731PubMedCrossRefGoogle Scholar
  14. Kohoutova J, Kuta Smatanova I, Brynda J, Lapkouski M, Revuelta JL, Arellano JB, Ettrich R (2009) Crystallization and preliminary crystallographic characterization of the extrinsic PsbP protein of photosystem II from Spinacia oleracea. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 2):111–115PubMedCentralPubMedCrossRefGoogle Scholar
  15. Komenda J, Nickelsen J, Tichy M, Prasil O, Eichacker LA, Nixon PJ (2008) The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 283(33):22390–22399PubMedCrossRefGoogle Scholar
  16. Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. Plant Cell 13(11):2539–2551PubMedCentralPubMedGoogle Scholar
  17. Levesque-Tremblay G, Havaux M, Ouellet F (2009) The chloroplastic lipocalin AtCHL prevents lipid peroxidation and protects Arabidopsis against oxidative stress. Plant J 60(4):691–702PubMedCrossRefGoogle Scholar
  18. Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci USA 103(33):12631–12636PubMedCentralPubMedCrossRefGoogle Scholar
  19. Liu J, Yang H, Lu Q, Wen X, Chen F, Peng L, Zhang L, Lu C (2012) PsbP-domain protein1, a nuclear-encoded thylakoid lumenal protein, is essential for photosystem I assembly in Arabidopsis. Plant Cell 24(12):4992–5006PubMedCentralPubMedCrossRefGoogle Scholar
  20. Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45(4):490–495PubMedCrossRefGoogle Scholar
  21. Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138(4):1903–1913PubMedCentralPubMedCrossRefGoogle Scholar
  22. Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281(46):35039–35047PubMedCrossRefGoogle Scholar
  23. Park HJ, Lee SS, You YN, Yoon DH, Kim BG, Ahn JC, Cho HS (2013) A rice immunophilin gene, OsFKBP16-3, confers tolerance to environmental stress in Arabidopsis and rice. Int J Mol Sci 14(3):5899–5919PubMedCentralPubMedCrossRefGoogle Scholar
  24. Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12(3):319–341PubMedCentralPubMedCrossRefGoogle Scholar
  25. Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T (2009) Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21(11):3623–3640PubMedCentralPubMedCrossRefGoogle Scholar
  26. Roose JL, Pakrasi HB (2008) The Psb27 protein facilitates manganese cluster assembly in photosystem II. J Biol Chem 283(7):4044–4050PubMedCrossRefGoogle Scholar
  27. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277(10):8354–8365PubMedCrossRefGoogle Scholar
  28. Sirpio S, Allahverdiyeva Y, Suorsa M, Paakkarinen V, Vainonen J, Battchikova N, Aro EM (2007) TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle. Biochem J 406(3):415–425PubMedCentralPubMedCrossRefGoogle Scholar
  29. Sirpio S, Khrouchtchova A, Allahverdiyeva Y, Hansson M, Fristedt R, Vener AV, Scheller HV, Jensen PE, Haldrup A, Aro EM (2008) AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II. Plant J 55(4):639–651PubMedCrossRefGoogle Scholar
  30. Spetea C, Lundin B (2012) Evidence for nucleotide-dependent processes in the thylakoid lumen of plant chloroplasts—an update. FEBS Lett 586(18):2946–2954PubMedCrossRefGoogle Scholar
  31. Spetea C, Hundal T, Lundin B, Heddad M, Adamska I, Andersson B (2004) Multiple evidence for nucleotide metabolism in the chloroplast thylakoid lumen. Proc Natl Acad Sci USA 101(5):1409–1414PubMedCentralPubMedCrossRefGoogle Scholar
  32. Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19(4):1347–1361PubMedCentralPubMedCrossRefGoogle Scholar
  33. Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010) The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J 62(2):240–249PubMedCrossRefGoogle Scholar
  34. Wang Y, Ma NN, Qiu SC, Zou HY, Zang GC, Kang ZH, Wang GX, Huang JL (2014) Regulation of the alpha-expansin gene OsEXPA8 expression affects root system architecture in transgenic rice plants. Mol Breed 34(1):47–57CrossRefGoogle Scholar
  35. Wangdi T, Uppalapati SR, Nagaraj S, Ryu CM, Bender CL, Mysore KS (2010) A role for chloroplast-localized Thylakoid Formation 1 (THF1) in bacterial speck disease development. Plant Signal Behav 5(4):425–427PubMedCentralPubMedCrossRefGoogle Scholar
  36. Wei L, Guo J, Ouyang M, Sun X, Ma J, Chi W, Lu C, Zhang L (2010) LPA19, a Psb27 homolog in Arabidopsis thaliana, facilitates D1 protein precursor processing during PSII biogenesis. J Biol Chem 285(28):21391–21398PubMedCentralPubMedCrossRefGoogle Scholar
  37. Wu HY, Liu MS, Lin TP, Cheng YS (2011) Structural and functional assays of AtTLP18.3 identify its novel acid phosphatase activity in thylakoid lumen. Plant Physiol 157(3):1015–1025PubMedCentralPubMedCrossRefGoogle Scholar
  38. Yabuta S, Ifuku K, Takabayashi A, Ishihara S, Ido K, Ishikawa N, Endo T, Sato F (2010) Three PsbQ-like proteins are required for the function of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell Physiol 51(6):866–876PubMedCrossRefGoogle Scholar
  39. Zou HY, Wenwen YH, Zang GC, Kang ZH, Zhang ZY, Huang JL, Wang GX (2015) OsEXPB2, a β-expansin gene, is involved in rice root system architecture. Mol Breed 35(1). doi: 10.1007/s11032-015-0203-y

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • ZhenHui Kang
    • 1
  • JunLi Huang
    • 1
  • HanYan Zou
    • 1
  • GuangChao Zang
    • 1
  • GuiXue Wang
    • 1
  1. 1.Key Laboratory of Biorheological Science and Technology (Chongqing University), Ministry of EducationBioengineering College of Chongqing UniversityChongqingChina

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