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Differential protein expression profiling of Arabidopsis thaliana callus under microgravity on board the Chinese SZ-8 spacecraft

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Exposure of Arabidopsis callus to microgravity has a significant impact on the expression of proteins involved in stress responses, carbohydrate metabolism, protein synthesis, intracellular trafficking, signaling, and cell wall biosynthesis.

Microgravity is among the main environmental stress factors that affect plant growth and development in space. Understanding how plants acclimate to space microgravity is important to develop bioregenerative life-support systems for long-term space missions. To evaluate the spaceflight-associated stress and identify molecular events important for acquired microgravity tolerance, we compared proteomic profiles of Arabidopsis thaliana callus grown under microgravity on board the Chinese spacecraft SZ-8 with callus grown under 1g centrifugation (1g control) in space. Alterations in the proteome induced by microgravity were analyzed by high performance liquid chromatography—electrospray ionization-tandem mass spectrometry with isobaric tags for relative and absolute quantitation labeling. Forty-five proteins showed significant (p < 0.05) and reproducible quantitative differences in expression between the microgravity and 1g control conditions. Of these proteins, the expression level of 24 proteins was significantly up-regulated and that of 21 proteins was significantly down-regulated. The functions of these proteins were involved in a wide range of cellular processes, including general stress responses, carbohydrate metabolism, protein synthesis/degradation, intracellular trafficking/transportation, signaling, and cell wall biosynthesis. Several proteins not previously known to be involved in the response to microgravity or gravitational stimuli, such as pathogenesis-related thaumatin-like protein, leucine-rich repeat extension-like protein, and temperature-induce lipocalin, were significantly up- or down-regulated by microgravity. The results imply that either the normal gravity-response signaling is affected by microgravity exposure or that microgravity might inappropriately induce altered responses to other environmental stresses.

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References

  • Abdallah C, Dumas-Gaudot E, Renaut J, Sergeant K (2012) Gel-base and gel-free quantitative proteomics approaches at a glance. Int J Plant Gen 2012:Article ID 494572

    Google Scholar 

  • Abebe T, Skadsen RW, Kaeppler HF (2005) A proximal upstream sequence controls tissue-specific expression of Lem2, a salicylate-inducible barley lectin-like gene. Planta 221:170–183

    Article  CAS  PubMed  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Babbick M, Dijkstra C, Larkin OJ, Anthony P, Davey MR, Power JB, Lowe KC, Cogoli-Greuter M, Hampp R (2007) Expression of transcription factors after short-term exposure of Arabidopsis thaliana cell cultures to hypergravity and simulated microgravity (2-D/3-D clinorotation, magnetic levitation). Adv Space Res 39:1182–1189

    Article  Google Scholar 

  • Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663

    Article  CAS  PubMed  Google Scholar 

  • Barjaktarovic Ž, Schütz W, Madlung J, Faladerer C, Nordheim A, Hampp R (2009) 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barjaktarović Z, Nordheim A, Lamkemeyer T, Fladerer C, Hampp R, Madlung J (2007) Time-course of changes in protein amounts of specific proteins upon exposure to hyper-g, 2-D clinorotation and random positioning of Arabidopsis cell cultures. J Exp Bot 58:4357–4363

    Article  PubMed  Google Scholar 

  • Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB (2008) A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. PNAS 105:4044–4049

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baumberger N, Ringli C, Keller B (2001) The chimeric leucine-rich repeat/extension cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Gene Dev 15:1128–1139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baumberger N, Doesseger B, Guyot R, Diet A, Parsons RL, Clark MA, Simmons MP, Bedinger P, Goff SA, Ringli C, Keller B (2003) Whole-genome comparison of leucine-rich repeat extensions in Arabidopsis and rice. A conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiol 131:1313–1326

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Claassen DE, Spooner BS (1994) Impact of altered gravity on aspects of cell biology. Int Rev Cyt 156:301–373

    Article  CAS  Google Scholar 

  • Dubois F, Tercé-Laforgue T, Gonzalez-Moro M-B, Estavillo J-M, Sangwan R, Gallais A, Hirel B (2003) Glutamate dehydrogenase in plants: is there a new story for an old enzyme? Plant Physiol Biochem 41:565–576

    Article  CAS  Google Scholar 

  • Fekete E, Seiboth B, Kubicek CP, Szentirmai A, Karaffa L (2008) Lack of aldose 1-epimerase in Hypocrea jecorina (anamorph Trichoderma reesei): a key to cellulose gene expression on lactose. PNAS 105:7141–7146

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ferl RJ, Zupanska A, Spinale A, Reed D, Manning-Roach S, Guerra G, Cox DR, Paul A-L (2011) The performance of KSC fixation tubes with RNAlater for orbital experiments: a case study in ISS operations for molecular biology. Adv Space Res 48:199–206

    Article  CAS  Google Scholar 

  • Foster JS, Wheeler RM, Pamphile R (2014) Host–microbe interactions in microgravity: assessment and implications. Life 4:250–266

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hausmann N, Fengler S, Hennig A, Franz-Wachtel M, Hampp R, Neef M (2014) Cytosolic 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

    Article  PubMed  Google Scholar 

  • Heese-Peck A, Raikhel NV (1998) The nuclear pore complex. Plant Mol Biol 38:145–162

    Article  CAS  PubMed  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57

    Article  CAS  Google Scholar 

  • Kamada M, Higashitani A, Ishioka N (2005) Proteomic analysis of Arabidopsis root gravitropism. Biol Sci Space 19:148–154

    Article  Google Scholar 

  • Keller BU, Hedrich R, Raschke K (1989) Voltage-dependent anion channels in the plasma membrane of guard cells. Nature 341:450–453

    Article  Google Scholar 

  • Kimbrough JM, Salinas-Mondragon R, Boss WF, Brown CS, Sederoff HW (2004) The fast and transient transcriptional net work of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 136:2790–2805

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Laurinavichius RS, Yaroshyus AV, Marchyukaytis A, Shvyaghdene DV, Mashinskiy AL (1986) Metabolism of pea plants grown under space flight conditions. USSR Space Life Sci Digest 4:23–25

    Google Scholar 

  • Leach JE, Ryba-White M, Sun Q, Wu CJ, Hilaire E, Gartner C, Nedukha O, Kordyum E, Keck M, Leung H, Guikerna JA (2001) Plants, plant pathogens, and microgravity—a deadly trio. Gravitat Space Biol Bull 14:15–23

    CAS  Google Scholar 

  • Leegood RC, Walker RP (2003) Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch Bichem Biophys 44:204–210

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  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 (2014) Microgravity induces changes in microsome-associated proteins of Arabidopsis seedlings grown on board the international space station. PLoS ONE 9:e91814

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Obenland DM, Brown CS (1994) The influence of altered gravity on carbohydrate metabolism in excised wheat leaves. J Plant Physiol 144:696–699

    Article  CAS  PubMed  Google Scholar 

  • Paul A-L, Daugherty CJ, Bihn EA, Chapman DK, Norwood KL, Ferl RJ (2001) Transgene expression patterns indicate that spaceflight affects stress signal perception and transduction in Arabidopsis. Plant Physiol 126:613–621

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paul AL, Levine HG, McLamb W, Norwood KL, Reed DW, Stutte GW, Wells HW, Ferl RJ (2005) Plant molecular biology in the space station era: utilization of KSC fixation tubes with RNAlater. Acta Astronaut 56:623–628

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Porterfield DM (2002) The biophysical limitations in physiological transport and exchange in plants grown in microgravity. J Plant Growth Regul 21:177–190

    Article  CAS  PubMed  Google Scholar 

  • Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR (1991) The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiol 95:509–516

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ryba-White M, Nedukha O, Hilaire E, Guikema JA, Kordyum E, Leach JE (2001) Growth in microgravity increases susceptibility of soybean to a fungal pathogen. Plant Cell Phyiol 42:657–664

    Article  CAS  Google Scholar 

  • Salinas T, Duchê A-M, Delage L, Nilsson S, Glaser E, Zaepfel M, Maréchal-Drouard L (2006) The voltage-dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. PNAS 103:18362–18367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shoshan-Barmatz V, Israelson A, Brdiczka D, Sheu SS (2006) The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr PhamDesign 2:2249–2270

    Article  Google Scholar 

  • Skagen EB, Iversen T-H (2000) Effect of simulated and real weightlessness on early regeneration stages of Brassica napus protoplasts. In Vitro Cell Dev Biol Plant 36:312–318

    Article  CAS  PubMed  Google Scholar 

  • Skopelitis DS, Paranychianakis NV, Paschalidis KA, Paliakonis ED, Delis LD, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. Plant Cell 18:2767–2781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stevenson-Paulik J, Love J, Boss WF (2003) Differential regulation of two Arabidopsis type III phosphatidylinositol 4-kinase isoforms. A regulatory role for the pleckstrin homology domain. Plant Physiol 132:1053–1064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stout SC, Porterfield DM, Briarty LG, Kuang A, Musgrave ME (2001) Evidence of root zone hypoxia in Brassica rapa L. grown in microgravity. Int J Plant Sci 162:249–255

    Article  CAS  PubMed  Google Scholar 

  • Stutte GW, Monje O, Hatfield RD, Paul AL, Ferl RJ, Simone CG (2006) Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat. Planta 224:1038–1049

    Article  CAS  PubMed  Google Scholar 

  • Subramanyam S, Sardesai N, Puthoff DP, Meyer JM, Nemacheck JA, Gonzalo M, Williams CE (2006) Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci 170:90–103

    Article  CAS  Google Scholar 

  • Tan C, Wang H, Zhang Y, Xu G, Bin Q, Zheng HQ (2011) Proteomic identification of differentially expressed proteins between Arabidopsis thaliana gravitropic insensitive mutant (pin 2) and wild type root tips under different gravitational conditions. Proteome Sci 9:72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Volkmann D, Buchen B, Hejnowicz Z, Tewinkel M, Sievers A (1991) Oriented movement of statoliths studied in a reduced gravitational field during parabolic flights of rockets. Planta 185:153–161

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Guo K, Gao D, Kang X, Jiang K, Li Y, Sun L, Zhang S, Sun C, Liu X, Wu W, Yang P, Liu Y (2011) Identification of transaldolase as a novel serum biomarker for hepatocellular carcinomametastasis using xenografted mouse model and clinic samples. Cancer Lett 313:154–166

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yong WD, Xu YY, Xu WZ, Wang X, Li N, Wu JS, Liang TB, Chong K, Xu ZH, Tan KH et al (2003) Vernalization-induced flowering in wheat is mediated by a lectin-like gene VER2. Planta 217:261–270

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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. 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).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

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

    Yue Zhang, Lihua Wang, Junyan Xie & Huiqiong Zheng

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  1. Yue Zhang
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  2. Lihua Wang
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  3. Junyan Xie
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  4. Huiqiong Zheng
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Correspondence to Huiqiong Zheng.

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Zhang, Y., Wang, L., Xie, J. et al. Differential protein expression profiling of Arabidopsis thaliana callus under microgravity on board the Chinese SZ-8 spacecraft. Planta 241, 475–488 (2015). https://doi.org/10.1007/s00425-014-2196-x

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