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The chloroplast outer membrane protein CHUP1 interacts with actin and profilin

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Abstract

Chloroplasts accumulate in response to low light, whereas high light induces an actin-dependent avoidance movement. This is a long known process, but its molecular base is barely understood. Only recently first components of the blue light perceiving signal cascade initiating this process were described. Among these, a protein was identified by the analysis of a deletion mutant in the corresponding gene resulting in a chloroplast unusual positioning phenotype. The protein was termed CHUP1 and initial results suggested chloroplast localization. We demonstrate that the protein is indeed exclusively and directly targeted to the chloroplast surface. The analysis of the deletion mutant of CHUP1 using microarray analysis shows an influence on the expression of genes found to be up-regulated, but not on genes found to be down-regulated upon high light exposure in wild-type. Analyzing a putative role of CHUP1 as a linker between chloroplasts and the cytoskeleton, we demonstrate an interaction with actin, which is independent on the filamentation status of actin. Moreover, binding of CHUP1 to profilin—an actin modifying protein—could be shown and an enhancing effect of CHUP1 on the interaction of profilin to actin is demonstrated. Therefore, a role of CHUP1 in bridging chloroplasts to actin filaments and a regulatory function in actin polymerization can be discussed.

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Abbreviations

Toc:

Translocon at the outer chloroplastic envelope membrane

PLP:

Poly-L-proline

PRM1:

Profilin-binding motif 1

References

  • Aparicio-Fabre R, Guillen G, Estrada G, Olivares-Grajales J, Gurrola G, Sanchez F (2006) Profilin tyrosine phosphorylation in poly-L-proline-binding regions inhibits binding to phosphoinositide 3-kinase in Phaseolus vulgaris. Plant J 47:491–500

    Article  PubMed  CAS  Google Scholar 

  • Böhm JA (1856) Beiträge zur näheren Kenntnis des Chlorophylls. SB Akad Wiss Wien Math Nat Kl 22:479–498

    Google Scholar 

  • Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes CR (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447

    Article  PubMed  CAS  Google Scholar 

  • Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR Görlach J (2001) Growth stage based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1520

    Article  PubMed  CAS  Google Scholar 

  • Diaz-Camino C, Villanueva MA (1999) Purification of multiple functional leaf-actin isoforms from Phaseolus vulgaris L. Biochem J 343:597–602

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Enguita FJ, Liras P, Leitão AL, Martín JF (1996) Interaction of the two proteins of the methoxylation system involved in cephamycin C biosynthesis. J Biol Chem 271:33225–33230

    Article  PubMed  CAS  Google Scholar 

  • Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ (2002) Functional plasticity of CH domains. FEBS Lett 513:98–106

    Article  PubMed  CAS  Google Scholar 

  • Harada A, Shimazaki K (2007) Phototropins and blue light-dependent calcium signaling in higher plants. Photochem Photobiol 8:102–111

    Article  CAS  Google Scholar 

  • Holt MR, Koffer A (2001) Cell motility: proline-rich proteins promote protrusions. Trends Cell Biol 11:38–46

    Article  PubMed  CAS  Google Scholar 

  • Jarillo JA, Gabrys H, Capel J, Alonso JM, Ecker JR, Cashmore AR (2001) Phototropin-related NPL1 controls chloroplast relocation induced by blue light. Nature 410:952–954

    Article  PubMed  CAS  Google Scholar 

  • Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291:2138–2141

    Article  PubMed  CAS  Google Scholar 

  • Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832

    Article  PubMed  CAS  Google Scholar 

  • Kong SG, Suzuki T, Tamura K, Mochizuki N, Hara-Nishimura I, Nagatani A (2006) Blue light-induced association of phototropin 2 with the Golgi apparatus. Plant J 45:994–1005

    PubMed  CAS  Google Scholar 

  • Kumatani T, Sakurai-Ozato N, Miyawaki N, Yokota E, Shimmen T, Terashima I, Takagi S (2006) Possible association of actin filaments with chloroplasts of spinach mesophyll cells in vivo and in vitro. Protoplasma 229(1):45–52

    Article  PubMed  CAS  Google Scholar 

  • Limmongkon A, Giuliani C, Valenta R, Mittermann I, Heberle-Bors E, Wilson C (2004) MAP kinase phosphorylation of plant profilin. Biochem Biophys Res Commun 324:382–386

    Article  PubMed  CAS  Google Scholar 

  • Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, Nishimura M (2004) Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol 43:331–341

    Article  Google Scholar 

  • Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M (2003) Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 15:2805–2815

    Article  PubMed  CAS  Google Scholar 

  • Peeters NM, Chapron A, Giritch A, Grandjean O, Lancelin D, Lhomme T, Vivrel A, Small I, (2000) Duplication and quadruplication of Arabidopsis thaliana cysteinyl- and asparaginyl-tRNA synthetase genes of organellar origin. J Mol Evol 50:413–423

    PubMed  CAS  Google Scholar 

  • Ritzenthaler C, Nebenführ A, Movafeghi A, Stussi-Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG (2002) Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14:237–261

    Article  PubMed  CAS  Google Scholar 

  • Sakai T, Kagawa T, Kasahara M, Swartz TE, Christie JM, Briggs WR, Wada M, Okada K (2001) Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc Natl Acad Sci USA 98:6969–6974

    Article  PubMed  CAS  Google Scholar 

  • Sathish K, Padma B, Munugalavadla V, Bhargavi V, Radhika KVN, Wasia R, Sairam M, Singh SS (2004) Phosphorylation of profilin regulates its interaction with actin and poly (L-proline). Cell Signal 16:589–596

    Article  PubMed  CAS  Google Scholar 

  • Schmidt von Braun S, Schleiff E (2007) Movement of endosymbiotic organelles. Curr Prot Pep Sci 8:426–438

    Article  Google Scholar 

  • Schleiff E, Soll J, Küchler M, Kühlbrandt W, Harrer R (2003) Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160:541–551

    Article  PubMed  CAS  Google Scholar 

  • Senn G (1908) Die Gestalts- und Lageveränderung der Pflanzen- Chromatophoren. Engelmenn, Leipzig

  • Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136:3968–3978

    Article  PubMed  CAS  Google Scholar 

  • Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Mol Cell Biol 5:198–208

    Article  PubMed  CAS  Google Scholar 

  • Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JA, Deng XW (2003) From seed to seed: the role of photoreceptors in Arabidopsis development. Dev Biol 260:289–297

    Article  PubMed  CAS  Google Scholar 

  • Vidali L, Perez HE, Valdés López V, Noguez R, Zamudio F, Sánchez F, (1995) Purification, characterization, and cDNA cloning of profilin from Phaseolus vulgaris. Plant Physiol 108:115–123

    Article  PubMed  CAS  Google Scholar 

  • Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1224–1231

    Article  PubMed  CAS  Google Scholar 

  • Wada M, Suetsugu N (2004) Plant organelle positioning. Curr Opin Plant Biol 7:626–631

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Pesacreta TC (2004) A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone subunit TCP-1alpha in maize. Cell Motil Cytoskel 57:218–232

    Article  CAS  Google Scholar 

  • Yarmola EG, Bubb MR (2006) Profilin: emerging concepts and lingering misconceptions, Trends Biochem Sci 4:197–205

    Article  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  PubMed  CAS  Google Scholar 

  • Zurzycki J (1955) Chloroplast arrangements as a factor of photosynthesis. Acta Soc Bot Pol 24:27–63

    Google Scholar 

Download references

Acknowledgements

We specially thank Prof. Chris Hawes from Oxford Brookes University for providing us with the Golgi marker ST-GFP (rat sialyl transferase fused to GFP, Boevink et al. 1998). This work was supported by grant to E.S. from the Volkswagenstiftung.

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Correspondence to Enrico Schleiff.

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Schmidt von Braun, S., Schleiff, E. The chloroplast outer membrane protein CHUP1 interacts with actin and profilin. Planta 227, 1151–1159 (2008). https://doi.org/10.1007/s00425-007-0688-7

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