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cyclo-Oxylipin-galactolipids in plants: occurrence and dynamics

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Abstract

cyclo-Oxylipin-galactolipids (cGL) are mono- or digalactosyldiglycerides carrying a cyclo-oxylipin in the sn1- and/or sn2-position or esterified to the galactose moiety. These compounds were recently identified in Arabidopsis thaliana. We provide evidence that cGL are mainly, if not exclusively, part of the thylakoid and can be hydrolysed by lipolytic activities associated with photosynthesis-related protein complexes in vitro. Using HPLC/ESI–mass spectrometry, cGL are shown to be restricted in occurrence to the genus Arabidopsis, they do not occur in other plants tested. A. thaliana cGL are rapidly and transiently formed upon wounding with characteristic changes in composition of the cGL-fraction. While the biological role of cGL is not understood, the genus Arabidopsis may present a model-case of chemical evolution of a novel class of regulatory molecules.

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Abbreviations

DGDG:

Digalactosyldiacylglycerol

cGL:

cyclo-Oxylipin-galactolipids

JA:

Jasmonic acid

LHCP:

Light harvesting complex protein

OPDA:

12-Oxophytodienoic acid

MGDG:

Monogalactosyldiacylglycerol

PG:

Phosphatidylglycerol

PSI (II):

Photosystem I (II)

TPT:

Triose phosphate translocator

References

  • Andersson MX, Hamberg M, Kourtchenko O, Brunnström Å, McPhail KL, Gerwick WH, Göbel C, Feussner I, Ellerström M (2006) Oxylipin-profiling of the hypersensitive response in Arabidopsis thaliana: formation of a novel oxo-phytodienoic acid containing galactolipid, arabidopside E. J Biol Chem 281:31528–31537

    Article  PubMed  CAS  Google Scholar 

  • Beckers GJM, Spoel SH (2005) Fine-tuning plant defence signalling: salicylate versus Jasmonate. Plant Biol 8:1–10

    Article  CAS  Google Scholar 

  • Blechert S, Brodschelm W, Hölder S, Kammerer L, Kutchan TM, Mueller MJ, Xia ZQ, Zenk MH (1995) The octadecanoic pathway: signal molecules for the regulation of secondary pathways. Proc Natl Acad Sci USA 92:4099–4105

    Article  PubMed  CAS  Google Scholar 

  • Buseman CM, Tamura P, Sparks AA, Baughman EJ, Maatta S, Zhao J, Roth MR, Wynn Esch S, Shah J, Williams TD, Welti R (2006) Wounding stimulates the accumulation of glycerolipids containing oxophytodienoic and dinor-oxophytodienoic acid in Arabidopsis leaves. Plant Physiol 142:28–39

    Article  PubMed  CAS  Google Scholar 

  • Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana—enzymes, products, regulation. Plant Biol 8:1–10

    Article  CAS  Google Scholar 

  • Demandre C, Tremolieres A, Justin AM, Mazliak P (1985) Analysis of molecular species of plant polar lipids by high-performance and gas liquid chromatography. Phytochemistry 24:481–485

    Article  CAS  Google Scholar 

  • Dörmann P, Hoffmann-Benning S, Balbo I, Benning C (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7:1801–1810

    Article  PubMed  Google Scholar 

  • Ferro M, Salvi D, Brugière S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  • Feussner I, Kuhn H, Wasternack C (2001) Lipoxygenase-dependent degradation of storage lipids. Trends Plant Sci 6:268–273

    Article  PubMed  CAS  Google Scholar 

  • Gounaris K, Whitford D, Barber J (1983) The effect of thylakoid lipids on an oxygen-evolving photosystem II preparation. FEBS Lett 163:230–234

    Article  CAS  Google Scholar 

  • Gundlach H, Zenk MH (1998) Biological activity and biosynthesis of pentacyclic oxylipins: the linoleic acid pathway. Phytochemistry 47:527–537

    Article  CAS  Google Scholar 

  • Guo J, Zhang Z, Bi Y, Yang W, Xu Y, Zhang L (2005) Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana. FEBS Lett 579:3619–3624

    Article  PubMed  CAS  Google Scholar 

  • Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97:10649–10654

    Article  PubMed  Google Scholar 

  • Hisamatsu Y, Goto N, Hasegawa K, Shigemori H (2003) Arabidopsides A and B, two new oxylipins from Arabidopsis thaliana. Tetrahedron Lett 44:5553–5556

    Article  CAS  Google Scholar 

  • Hisamatsu Y, Goto N, Sekiguchi M, Hasegawa K, Shigemori H (2005) Oxylipins arabidopsides C and D from Arabidopsis thaliana. J Nat Prod 68:600–603

    Article  PubMed  CAS  Google Scholar 

  • Hisamatsu Y, Goto N, Hasegawa K, Shigemori H (2006) Senescence-promoting effects of arabidopside A. Z Naturforsch 61:363–366

    CAS  Google Scholar 

  • Ishiguro S, Kwai-Oda A, Ueda J, Nishida I, Okada K (2001) The defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation. Plant Cell 13:2191–2209

    Article  PubMed  CAS  Google Scholar 

  • Jarvis P, Dörmann P, Charles AP, Jason L, Beninng C, Joanne C (2000) Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97:8175–8179

    Article  PubMed  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917

    Article  PubMed  CAS  Google Scholar 

  • Joyard J, Maréchal E, Block MA, Douce R (1996) Plant galactolipids and sulfolipid: structure, distribution and biosynthesis. In: Smallwood M, Knox P, Bowles DJ (ed) Membranes: specialized functions in plants. BIOS Scientific Publishers, Oxford, pp 179–194

    Google Scholar 

  • Krupa Z, Baszynski T (1975) Requirement of galactolipids for photosystem I activity in lyophilized spinach chloroplasts. Biochim Biophys Acta 408:26–34

    Article  PubMed  CAS  Google Scholar 

  • Kunst L (1998) Preparation of physiologically active chloroplasts from Arabidopsis. In: Martinez-Zapater JM, Salinas J (eds) Methods in molecular biology, Arabidopsis protocols, vol. 82. Humana Press, Totowa, pp 43–48

  • Kutchan TM (1993) 12-Oxo-phytodienoic acid induces accumulation of berberine bridge enzyme transcripts in a manner analogous to methyl jasmonate. J Plant Physiol 142:502–505

    CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684

    Article  PubMed  CAS  Google Scholar 

  • Laudert D, Pfannschmidt U, Lottspeich F, Holländer-Czytko H, Weiler EW (1996) Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates. Plant Mol Biol 31:323–335

    Article  PubMed  CAS  Google Scholar 

  • Li HM, Moore T, Keegstra K (1991) Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell 3:709–717

    Article  PubMed  CAS  Google Scholar 

  • Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292

    Article  PubMed  CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044

    Article  PubMed  CAS  Google Scholar 

  • Murata N, Fujimura Y, Higashi S (1990) Glycerolipids in various preparations of photosystem II from spinach chloroplasts. Biochim Biophys Acta 1019:261–268

    Article  CAS  Google Scholar 

  • Nussberger S, Dörr K, Wang DN, Kuhlbrandt W (1993) Lipid–protein interactions in crystals of plant light-harvesting complex. J Mol Biol 234:347–356

    Article  PubMed  CAS  Google Scholar 

  • Pick U, Weiss M, Gounaris K, Barber J (1987) The role of different thylakoid glycolipids in the function of reconstituted chloroplasts ATP synthase. Biochim Biophys Acta 891:28–39

    Article  CAS  Google Scholar 

  • Schägger H, von Jagow G (1991) Blue-native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231

    Article  PubMed  Google Scholar 

  • Schaller F, Schaller A, Stinzi A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Google Scholar 

  • Schleiff E, Klösgen RB (2001) Without a little help from my friends: direct insertion of proteins into chloroplast membranes? Biochim Biophys Acta 1541:22–33

    Article  PubMed  CAS  Google Scholar 

  • Steffen R, Kelly AA, Huyer J, Dörmann P, Renger G (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44:3134–3142

    Article  PubMed  CAS  Google Scholar 

  • Stelmach BA, Müller A, Hennig P, Laudert D, Andert L, Weiler EW (1997) Quantitation of the octadecanoid 12-oxo-phytodienoic acid, a signalling compound in plant mechanotransduction. Phytochemistry 47:539–546

    Article  Google Scholar 

  • Stelmach BA, Müller A, Hennig P, Gebhardt S, Schubert-Zsilavecz M, Weiler EW (2001) A novel class of oxylipins, sn1-O-(12-oxophytodienoyl)-sn2-O-(hexadecatrienoyl)-monogalactosyl diglyceride from Arabidopsis thaliana. J Biol Chem 276:12832–12838

    Article  PubMed  CAS  Google Scholar 

  • Stinzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98:12837–12842

    Article  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b6f complex. Nature 426:413–418

    Article  PubMed  CAS  Google Scholar 

  • Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H (2005) 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139:1268–1283

    Article  PubMed  CAS  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamid gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Article  PubMed  CAS  Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell Suppl S153-S164

  • Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dörmann P, Kessler F, Bréhélin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234

    Article  PubMed  CAS  Google Scholar 

  • Weiler EW, Albrecht T, Groth B, Xia ZQ, Luxem M, Liß H, Andert L, Spengler P (1993) Evidence for the involvement of jasmonates and their octadecanoid precursors in the tendril coiling response of Bryonia dioica. Phytochemistry 32:591–600

    Article  CAS  Google Scholar 

  • Ytterberg AJ, Peltier JB, van Wijk KJ (2006) Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol 140:984–997

    Article  PubMed  CAS  Google Scholar 

  • Zerbe P, Weiler EW, Schaller F (2007) Preparative enzymatic solid phase synthesis of cis(+)-12-oxo-phytodienoic acid–physical interaction of AOS and AOC is not necessary. Phytochemistry 68:229–236

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Jun-Prof. Danja Schünemann (Lehrstuhl für Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, Germany) for providing the LHCP and cpSRP43 antibodies as well as the secondary antibody from chicken. We also like to thank Prof. Ulf-Ingo Flügge (Lehrstuhl für Botanik II, Universität zu Köln, Germany) for the kind provision of the TPT antibody. Furthermore we thank Dr. Markus Piotrowski (Lehrstuhl für Pflanzenphysiologie, Ruhr-Universität Bochum, Germany) for the mass spectrometrical analyses of the thylakoid protein complexes. This work was funded by a grant of the Deutsche Forschungsgemeinschaft (SFB480, TP A8) to EWW.

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Correspondence to Christine Böttcher.

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Böttcher, C., Weiler, E.W. cyclo-Oxylipin-galactolipids in plants: occurrence and dynamics. Planta 226, 629–637 (2007). https://doi.org/10.1007/s00425-007-0511-5

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