Planta

, Volume 229, Issue 4, pp 767–779 | Cite as

Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes

Original Article

Abstract

In land plants plastocyanin is indispensable and therefore copper (Cu) availability is a prerequisite for growth. When Cu supply is limited, higher plants prioritize the Cu delivery to plastocyanin by down-regulation of other Cu proteins. Arabidopsis has two plastocyanin genes (PETE1 and PETE2). PETE2 is the predominant isoform in soil-grown plants and in hydroponic cultures it is accumulated in response to Cu addition. It functions as a Cu sink when more Cu is available, in addition to its role as an electron carrier. PETE1 is not affected by Cu feeding and it is the isoform that drives electron transport under Cu-deficiency. Cu feeding rescued the defect in photosystem II electron flux (ΦPSII) in the pete1 mutant whereas ΦPSII was not changed in the pete2 mutant as Cu was added. Plants with mutations in the plastocyanin genes had altered Cu homeostasis. The pete2 mutant accumulated more Cu/Zn superoxide dismutase (CSD2 and CSD1) and Cu chaperone (CCS) whereas the pete1 mutant accumulated less. On the other hand, less iron superoxide dismutase (FeSOD) and microRNA398b were observed in the pete2 mutant, whereas more were accumulated in the pete1 mutant. Our data suggest that plastocyanin isoforms are different in their response to Cu and the absence of either one changes the Cu homeostasis. Also a small amount of plastocyanin is enough to support efficient electron transport and more PETE2 is accumulated as more Cu is added, presumably, to buffer the excess Cu.

Keywords

Arabidopsis Copper homeostasis Plastocyanin isoforms Superoxide dismutase 

Abbreviations

CCS

Copper chaperone for superoxide dismutase

CSD1

Cu/Zn superoxide dismutase 1

CSD2

Cu/Zn superoxide dismutase 2

FeSOD

Iron superoxide dismutase

ΦPSII

Electron flux through photosystem II

miRNA

MicroRNA

NPQ

Non-photochemical quenching

PETE1

Plastocyanin 1

PETE2

Plastocyanin 2

PQ

Plastoquinone

PSI

Photosystem I

Rbc-L

Large subunit of the ribulose-bisphosphate carboxylase

Rbc-S

Small subunit of the ribulose-bisphosphate carboxylase

Supplementary material

425_2008_869_MOESM1_ESM.tif (6.5 mb)
Supplementary Fig. S1 (TIFF 2560 kb)
425_2008_869_MOESM2_ESM.tif (2.5 mb)
Supplementary Fig. S2 (TIFF 6649 kb)

References

  1. Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945PubMedCrossRefGoogle Scholar
  2. Abdel-Ghany SE, Burkhead JL, Gogolin KA, Andres-Colas N, Bodecker JR, Puig S, Penarrubia L, Pilon M (2005a) AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett 579:2307–2312PubMedCrossRefGoogle Scholar
  3. Abdel-Ghany SE, Muller-Moule P, Niyogi KK, Pilon M, Shikanai T (2005b) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251PubMedCrossRefGoogle Scholar
  4. Alt J, Westhoff P, Sears BB, Nelson N, Hurt E, Hauska G, Herrmann RG (1983) Genes and transcripts for the polypeptides of the cytochrome b6/f complex from spinach thylakoid membranes. EMBO J 2:979–986PubMedGoogle Scholar
  5. Andersson U, Heddad M, Adamska I (2003) Light stress-induced one-helix protein of the chlorophyll a/b-binding family associated with photosystem I. Plant Physiol 132:811–820PubMedCrossRefGoogle Scholar
  6. Beauchamp C, Fridovich I (1971) Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287PubMedCrossRefGoogle Scholar
  7. Bichler J, Herrmann RG (1990) Analysis of the promotors of the single-copy genes for plastocyanin and subunit delta of the chloroplast ATP synthase from spinach. Eur J Biochem 190:415–426PubMedCrossRefGoogle Scholar
  8. Bradford M (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  9. Briggs LM, Pecoraro VL, McIntosh L (1990) Copper-induced expression, cloning, and regulatory studies of the plastocyanin gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 15:633–642PubMedCrossRefGoogle Scholar
  10. Clarke AK, Campbell D (1996) Inactivation of the petE gene for plastocyanin lowers photosynthetic capacity and exacerbates chilling-induced photoinhibition in the cyanobacterium Synechococcus. Plant Physiol 112:1551–1561PubMedCrossRefGoogle Scholar
  11. Cohu CM, Pilon M (2007) Regulation of superoxide dismutase expression by copper availability. Physiol Plant 129:747–755CrossRefGoogle Scholar
  12. Dimitrov MI, Donchev AA, Egorov TA (1993) Twin plastocyanin dimorphism in tobacco. Biochim Biophys Acta 1203:184–190PubMedGoogle Scholar
  13. Himelblau E, Amasino RM (2001) Nutrients mobilization from leaves of Arabidopsis thaliana during leaf senescence. J of Plant Physiol 158:1317–1323CrossRefGoogle Scholar
  14. Hoagland DR, Arnon DI (1938) The water culture method for growing plants without soil. University of California, College of Agriculture Experimental Station Circular, Berkely, pp 347–353Google Scholar
  15. Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368PubMedCrossRefGoogle Scholar
  16. Kieselbach T, Hagman A, Andersson B, Schroder WP (1998) The thylakoid lumen of chloroplasts. Isolation and characterization. J Biol Chem 273:6710–6716PubMedCrossRefGoogle Scholar
  17. Kieselbach T, Bystedt M, Hynds P, Robinson C, Schroder WP (2000) A peroxidase homologue and novel plastocyanin located by proteomics to the Arabidopsis chloroplast thylakoid lumen. FEBS Lett 480:271–276PubMedCrossRefGoogle Scholar
  18. Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650PubMedCrossRefGoogle Scholar
  19. Knoetzel J, Mant A, Haldrup A, Jensen PE, Scheller HV (2002) PSI-O, a new 10-kDa subunit of eukaryotic photosystem I. FEBS Lett 510:145–148PubMedCrossRefGoogle Scholar
  20. Kusnetsov V, Bolle C, Lubberstedt T, Sopory S, Herrmann RG, Oelmuller R (1996) Evidence that the plastid signal and light operate via the same cis-acting elements in the promoters of nuclear genes for plastid proteins. Mol Gen Genet 252:631–639PubMedGoogle Scholar
  21. Last DI, Gray JC (1990) Synthesis and accumulation of pea plastocyanin in transgenic tobacco plants. Plant Mol Biol 14:229–238PubMedCrossRefGoogle Scholar
  22. Li HM, Theg SM, Bauerle CM, Keegstra K (1990) Metal-ion-center assembly of ferredoxin and plastocyanin in isolated chloroplasts. Proc Natl Acad Sci USA 87:6748–6752PubMedCrossRefGoogle Scholar
  23. Li HH, Quinn J, Culler D, Girard-Bascou J, Merchant S (1996) Molecular Genetic Analysis of Plastocyanin Biosynthesis in Chlamydomonas reinhardtii. J Biol Chem 271:31283–31289PubMedCrossRefGoogle Scholar
  24. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668PubMedCrossRefGoogle Scholar
  25. Merchant S, Bogorad L (1987) Metal ion regulated gene expression: use of a plastocyanin-less mutant of Chlamydomonas reinhardtii to study the Cu(II)-dependent expression of cytochrome c-552. The EMBO Journal 6:2531–2535PubMedGoogle Scholar
  26. Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochimica et Biophysica Acta 1763:578–594PubMedGoogle Scholar
  27. Muller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedCrossRefGoogle Scholar
  28. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  29. Pesaresi P, Scharfenberg M, Weigel M, Granlund I, Schroder WP, Finazzi G, Rappaport F, Masiero S, Furini A, Jahns P, Leister D (2008) Mutants, overexpressors, and interactors of Arabidopsis plastocyanin isoforms: revised roles of plastocyanin in photosynthetic electron flow and thylakoid redox state. Mol Plant: 1–13. doi:10.1093/mp/ssn041
  30. Pfannschmidt T, Schutze K, Brost M, Oelmuller R (2001) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276:36125–36130PubMedCrossRefGoogle Scholar
  31. Philippar K, Geis T, Ilkavets I, Oster U, Schwenkert S, Meurer J, Soll J (2007) Chloroplast biogenesis: the use of mutants to study the etioplast–chloroplast transition. Proc Natl Acad Sci USA 104:678–683PubMedCrossRefGoogle Scholar
  32. Pilon M, Abdel-Ghany SE, Cohu CM, Gogolin KA, Ye H (2006) Copper cofactor delivery in plant cells. Curr Opin Plant Biol 9:256–263PubMedCrossRefGoogle Scholar
  33. Quinn JM, Merchant S (1998) Copper-responsive gene expression during adaptation to copper deficiency. Methods Enzymol 297:263–279PubMedCrossRefGoogle Scholar
  34. Quinn J, Li HH, Singer J, Morimoto B, Mets L, Kindle K, Merchant S (1993) The plastocyanin-deficient phenotype of Chlamydomonas reinhardtii Ac-208 results from a frame-shift mutation in the nuclear gene encoding preapoplastocyanin. J Biol Chem 268:7832–7841PubMedGoogle Scholar
  35. Raven JA, Evans MC, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149CrossRefGoogle Scholar
  36. Rensing SA et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:64–69PubMedCrossRefGoogle Scholar
  37. Schlarb-Ridley BG, Nimmo RH, Purton S, Howe CJ, Bendall DS (2006) Cytochrome c(6A) is a funnel for thiol oxidation in the thylakoid lumen. FEBS Lett 580:2166–2169PubMedCrossRefGoogle Scholar
  38. 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 277:8354–8365PubMedCrossRefGoogle Scholar
  39. Schutze K, Steiner S, Pfannschmidt T (2008) Photosynthetic redox regulation of the plastocyanin promoter in tobacco. Physiol Plant 133:557–565PubMedCrossRefGoogle Scholar
  40. Shikanai T, Muller-Moule P, Munekage Y, Niyogi KK, Pilon M (2003) PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts. Plant Cell 15:1333–1346PubMedCrossRefGoogle Scholar
  41. Shosheva A, Donchev A, Dimitrov M, Kostov G, Toromanov G, Getov V, Alexov E (2005) Comparative study of the stability of poplar plastocyanin isoforms. Biochim Biophys Acta 1748:116–127PubMedGoogle Scholar
  42. Takabe T, Takabe T, Akazawa T (1986) Biosynthesis of P700-chlorophyll a protein complex, plastocyanin, and cytochrome b(6)/f Complex. Plant Physiol 81:60–66PubMedCrossRefGoogle Scholar
  43. Van Camp W, Capiau K, Van Montagu M, Inze D, Slooten L (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol 112:1703–1714PubMedCrossRefGoogle Scholar
  44. Vorst O, Kock P, Lever A, Weterings B, Weisbeek P, Smeekens S (1993) The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J 4:933–945PubMedCrossRefGoogle Scholar
  45. Wastl J, Bendall DS, Howe CJ (2002) Higher plants contain a modified cytochrome c(6). Trends Plant Sci 7:244–245PubMedCrossRefGoogle Scholar
  46. Waters BM, Grusak MA (2008) Quantitative trait locus mapping for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. New Phytol 179:1033–1047PubMedCrossRefGoogle Scholar
  47. Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289PubMedCrossRefGoogle Scholar
  48. Wintermans JF, De Mots A (1965) Spectrophotometric characteristics of chlorophyll a and b and their pheophytins in ethanol. Biochem Biophys Acta 109:448–453PubMedCrossRefGoogle Scholar
  49. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378PubMedCrossRefGoogle Scholar
  50. Zhang L, McSpadden B, Pakrasi HB, Whitmarsh J (1992) Copper-mediated regulation of cytochrome c553 and plastocyanin in the cyanobacterium Synechocystis 6803. J Biol Chem 267:19054–19059PubMedGoogle Scholar
  51. Zhang L, Pakrasi HB, Whitmarsh J (1994) Photoautotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803 in the absence of cytochrome c553 and plastocyanin. J Biol Chem 269:5036–5042PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Biology Department, Program in Molecular Plant BiologyColorado State UniversityFort CollinsUSA
  2. 2.Botany Department, Faculty of ScienceZagazig UniversityZagazigEgypt

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