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Changes in Plastid and Mitochondria Protein Expression in Arabidopsis Thaliana Callus on Board Chinese Spacecraft SZ-8

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Abstract

Microgravity represents an adverse abiotic environment, which causes rearrangements in cellular organelles and changes in the energy metabolism of cells. Plastids and mitochondria are two subcellular energy organelles that are responsible for major metabolic processes, including photosynthesis, oxidative phosphorylation, ß-oxidation, and the tricarboxylic acid cycle. In our previous study performed on board the Chinese spacecraft SZ-8, we evaluated the global changes exerted by microgravity on the proteome of Arabidopsis thaliana cell cultures by comparing the microgravity-exposed samples with the controls either under 1 g centrifugation in space or 1 g ground conditions. Here, we report additional data from this space experiment that highlights the plastid and mitochondria proteins that responded to space flight conditions. We observed that 43 plastidial proteins and 50 mitochondrial proteins changed their abundances under microgravity in space. The major changes in both plastids and mitochondria involved proteins that functions in a suite of redox antioxidant and metabolic pathways. These results suggested that these antioxidant and metabolic changes in plastids and mitochondria could be important components of the adaptive strategy in plants subjected to microgravity in space.

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References

  • Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol 55, 373–399 (2004)

    Article  Google Scholar 

  • Barjaktarovic, Z., Schütz, W., Madlung, J., Faladerer, C., Nordheim, A., Hampp, R.: Changes in the effective gravitational field strength affect the state of phosphorylation of stress-related proteins in callus cultures of Arabidopsis thaliana. J. Exp. Bot 60, 779–789 (2009)

    Article  Google Scholar 

  • Behal, R.H., Oliver, D.J.: NAD +-dependent isocitrate dehydrogenase from Arabidopsis thaliana. Characterization of two closely related subunits. Plant Mol. Biol 36, 691–698 (1998)

    Article  Google Scholar 

  • Blée, E., Boachon, B., Burcklen, M., Guédard, M.L., Hanano, A., Heintz, D., Ehlting, J., Herrfurth, C., Feussner, I., Bessoule, J-J.: The reductase activity of the Arabidopsis caleosin RESPONSIVE TO DESSICATION20 mediates gibberllin-dependent flowering time, abscisic acid sensitivity, and tolerance to oxidative stress. Plant Physiol. 166, 109–124 (2014)

    Article  Google Scholar 

  • Brown, C.S., Piastuch, W.C.: Starch metabolism in germinating soybean cotyledons is sensitive to clinorotation and centrifugation. Plant Cell Environ 17, 341–344 (1994)

    Article  Google Scholar 

  • Chang, C., Slesak, I., Jordá, L., Sotnikov, A., Melzer, M., Miszalski, Z., Mullineaux, P.M., Parker, J.E., Karpinska, B., Karpinski, S.: Arabidopsis chloroplastid glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol. 150, 670–683 (2009)

    Article  Google Scholar 

  • Cortleven, A., Nitschke, S., Klaumünzer, M., AbdElgawad, H., Asard, H., Grimm, B., Riefler, M., Schmülling, T.: A novel protective function for cytokinin in the light stress response is mediated by the Arabidopsis histidine kinase2 and Arabidopsis histidine kinase3 receptors. Plant Physiol 164, 1470–1483 (2014)

    Article  Google Scholar 

  • De Micco, V., De Pascale, S., Paradiso, R., Aronne, G.: Microgravity effects on different stages of higher plant life cycle and completion of the seed-to seed cycle. Plant Biol. 16, 31–38 (2014)

    Article  Google Scholar 

  • Ferl, R., Wheeler, R., Levine, H.G., Paul, A-L.: Plants in space. Curr. Opin. Plant Biol. 5, 258–263 (2001)

    Article  Google Scholar 

  • Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J-B., Rudella, A., Sun, Q., van Wijk, KJ.: In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions and a plastid proteome database. Plant Cell. 16, 478–499 (2004)

    Article  Google Scholar 

  • Gakh, O., Cavadini, P., Isaya, G.: Mitochondrial processing peptidases, vol. 1592, pp 63–77 (2002)

  • Galvis, M.E., Marttila, S., Håkansson, G., Forsberg, J., Knorpp, C.: Heat stress response in pea involves interaction of mitochondrial nucleoside diphosphate kinase with a novel 86-kilodalton protein. Plant Physiol. 126, 69–77 (2001)

    Article  Google Scholar 

  • Hampp, R., Hoffmann, E., Schönherr, K., Johann, P., Filippis, L.E.: Fusion and metabolism of plant cells as affected by microgravity. Planta 203, S42–S53 (1997)

    Article  Google Scholar 

  • Hausmann, N., Fengler, S., Hennig, A., Franz-Wachtel, M., Hampp, R., Neef, M.: Cytosoli calcium, hydrogen peroxide and related gene expression and protein modulation in Arabidopsis thaliana cell cultures respond immediately to altered gravitation: parabolic flight data. Plant Biol. 16, 120–128 (2014)

    Article  Google Scholar 

  • Hossain, M.A., Nakano, Y., Asada, K.: Monodehydroascorbate reductase in spinach chloroplast and its participation in regeneration of ascorbate for scavenging of hydrogen peroxide. Plant Cell Physiol. 25, 385–39 (1984)

    Google Scholar 

  • Igamberdiev, A.U., Gardeström, P.: Regulation of NAD-and NADP-dependent isocitrate dehydrogenases by reduction levels of pyridine nucleotides in mitochondria and cytosol of pea leaves. Biochimica. Et. Biophysica. Acta 1606, 117–125 (2003)

    Article  Google Scholar 

  • Kim, H.J., Park, J-W.: Oxalomalate, a competitive inhibitor of NADP + -dependent isocitrate dehydrogenase, regulates heat shock-induced apoptosis. Biochem. Biophys. Res. Commun 337, 685–691 (2005)

    Article  Google Scholar 

  • Kim, J., Olinares, P.D., Oh, S-h., Ghisaura, S., Poliakov, A., Ponnala, L., van Wijk, K.J.: Modified Clp protease complex in the ClpP3 null mutant and consequences for chloroplast development and function in Arabidopsis. Plant Physiol 162, 157–179 (2013)

    Article  Google Scholar 

  • Kordyum, E.L.: Plant cell gravisensitivity and adaptation to microgravity. Plant Bio. 16, 79–90 (2014)

    Article  Google Scholar 

  • Kozeko, L., Kordyum, E.: Effect of hypergravity on the level of heat shock proteins 70 and 90 in pea seedlings. Microgravity Sci Technol. 21, 175–178 (2009)

    Article  Google Scholar 

  • Laurinavichius, R.S., Yaroshyus, A.V., Marchyukaytis, A., Shvyaghdene, D.V., Mashinskiy, A L: Metabolism of pea plants grown under space flight conditions. USSR Space Life Sci. Digest 4, 23–25 (1986)

    Google Scholar 

  • Less, H., Galili, G.: Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 147, 316–330 (2008)

    Article  Google Scholar 

  • Martzivanou, M., Hampp, R.: Hyper-gravity effects on the Arabidopsis transcriptome. Physiol. Plantarum 118, 221–231 (2003)

    Article  Google Scholar 

  • Matía, I., González-Camacho, F., Herranz, R., Kiss, J.Z., Gasset, G., van Loon, J., MarCo, R., Medina, F.J.: Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. J. Plant Physiol. 167, 184–193 (2010)

    Article  Google Scholar 

  • Mazars, C., Brière, C., Grat, S., Pichereaux, C., Rossignol M., Pereda-Loth, V., Eche, B., Boucheron-Dubisson, E., Disquet, IL., Medina, FJ., Graziana, A., Carnero-Diaz E.: Microgravity induces changes in microsome-associated proteins of Arabidopsis seedlings grown on board the international space station. PLoS. ONE 9(3), e91814 (2014)

    Article  Google Scholar 

  • Meleshko, G.I., Anton’yan, A.A., Sycheyev, V.N., Solontsova, I.P., Shetlik, I., Doukha, Y.: The effect of space flight factors on the pigment system of one-celled algae. USSR Space Life Sci. Digest 31, 43–45 (1991)

    Google Scholar 

  • Moore, R., Fondren, W.M., Marcum, H.: Characterization of root agravitropism induced by genetic, chemical, and developmental constraints. Am. J. Bot 74, 329–336 (1987)

    Article  Google Scholar 

  • Mu, J., Tan, H., Zheng, Q., Fu, F., Liang, Y., Zhang, J., Yang, X., Wang, T., Chong, K., Wang, X-J., Zuo, J.: Leafy cotyledon1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 148, 1042–1054 (2008)

    Article  Google Scholar 

  • Musgrave, M. E.: Seeds in space. Seed Sci. Res. 12, 1–17 (2002)

    Article  Google Scholar 

  • Nury, H., Dahout-Gonzalez, C., Trézéguet, V., Lauquin, G.J., Brandolin, G., Pebay-Peyroula, E.: Relations between structure and function of the mitochondrial ADP/ATP carrier. Annu. Rev. Biochem 75, 713–741 (2006)

    Article  Google Scholar 

  • Parks Jr., R.E, Agarwal, R.P.: Nucleoside diphosphokinase. In: P.D Boyer (ed.) : The Enzymes. Vol. 8, pp 309–313. Academic Press, New York (1973)

  • Paul, A.L., Levine, H.G., McLamb, W., Norwood, K.L., Reed, D.W., Stutte, G.W., Wells, H.W., Ferl, R.J.: Plant molecular biology in the space station era: utilization of KSC fixation tubes with RNAlater. Acta. Astronaut 56, 623–628 (2005)

    Article  Google Scholar 

  • Paul, A-L., Daugherty, C.J., Bihn, E.A., Chapman, D.K., Norwood, K.L., Ferl, R.J.: Transgene expression patterns indicate that spaceflight affects stress signal perception and transduction in Arabidopsis. Plant Physiol. 126, 613–621 (2001)

    Article  Google Scholar 

  • Paul, A-L., Wheeler, R.M., Levine, H.G., Ferl, R.J.: Fundamental plant biology enable by the space shuttle. Amer. J. Bot. 100, 226–234 (2013)

    Article  Google Scholar 

  • Phelps, A., Briggs, C., Mincone, L., Wohlrab, H.: Mitochondrial phosphate transport protein. replacements of glutamic, aspartic, and histidine residues affect transport and protein conformation and point to a coupled proton transport path. Biochemistry 20;35(33), 10757–10762 (1996)

    Article  Google Scholar 

  • Popova, A.F.: Comparative charactreristic of mitochondria ultrastructural organization in Chalorella cells under altered gravity conditions. Adv. Space Res. 31, 2253–2259 (2003)

    Article  Google Scholar 

  • Roosens, N., Al-Bitar, F.A., Jacobs, M., Homble, F.: Characterization of a cDNA encoding a rice mitochondrial voltage-depedent anion channel and its gene expression studied upon plant development and osmotic stress. Biochim. Biophys. Acta 1463, 470–476 (2000)

    Article  Google Scholar 

  • Stein, T.P., Leskiw, M.J.: Oxidant damage during and after spaceflight. Am. J. Physiol. Endocrinol. Metab. 278, 375–382 (2000)

    Google Scholar 

  • Sun, L., Zhang, Q., Wu, J., Zhang, L., Jiao, X., Zhang, S., Zhang, Z., Sun, D., Lu, T., Sun, Y.: Two ric authentic histidine phospotransfer proteins, OsAHP1 and OsAHP2, mediate cytokinin signaling and stress responses in rice. Plant Physiol. 165, 335–345 (2014)

    Article  Google Scholar 

  • Taylor, N.L., Tan, Y.F., Jacoby, R.P., Millar, A.H.: Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteomics 72, 367–378 (2009)

    Article  Google Scholar 

  • Vasilenko, A., Popova, A.F.: Energetic metabolism response in algae and higher plant species from simulation experiments with the clinostat. Adv. Space Res 17, 103–106 (1996)

    Article  Google Scholar 

  • Wolff, S.A., Coelho, L.H., Zabrodina, M., Brinckmann, E., Kittang A-I.: Plant mineral nutrition, gas exchange and photosynthesis in space: a review. Adv. Space Res. 51, 465–475 (2013)

    Article  Google Scholar 

  • Wang, H., Zheng, H.Q., Sha, W., Zeng, R., Xia, Q.C.: A proteomic approach to analysing responses of Arabidopsis thaliana callus cells to clinostat rotation. J. Exp. Bot 57, 827–835 (2006)

    Article  Google Scholar 

  • Zhang, Y., Wang, L., Xie, J., Zheng, H.Q.: Differential protein expression profiling of Arabidopsis thaliana callus under microgravity on board the Chinese SZ-8 spacecraft. Planta 241(2), 475–488 (2015)

    Article  Google Scholar 

  • Zupanska, A.K., Denison, F.C., Ferl, R.J., Paul, A.-L.: Spaceflight engages heat shock protein and other molecular chaperone genes in tissues culture cells of Arabidopsis thaliana. Am. J. Bot 100, 235–248 (2013)

    Article  Google Scholar 

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Acknowledgments

The authors are indebted to Astrium Space Transportation in Germany for SIMBOX construction and Dr. Markus Braun for helping in the space experiment, Prof. Hampp for helpful suggestions and comments on the experiment. This work was supported by the National Basic Research Program of China (2011CB710902), the China Manned Space Flight Technology project, and the Strategic Pioneer Projects of CAS (XDA04020202).

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The authors declare that they have no conflict of interest.

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  1. Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China

    Yue Zhang & Hui Qiong Zheng

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  1. Yue Zhang
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Correspondence to Hui Qiong Zheng.

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Zhang, Y., Zheng, H.Q. Changes in Plastid and Mitochondria Protein Expression in Arabidopsis Thaliana Callus on Board Chinese Spacecraft SZ-8. Microgravity Sci. Technol. 27, 387–401 (2015). https://doi.org/10.1007/s12217-015-9431-3

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