Gene expression changes induced by space flight in single-cells of the fern Ceratopteris richardii

Abstract

This work describes a rare high-throughput evaluation of gene expression changes induced by space flight in a single plant cell. The cell evaluated is the spore of the fern Ceratopteris richardii, which exhibits both perception and response to gravity. cDNA microarray and Q RT-PCR analysis of spores germinating in microgravity onboard NASA space shuttle flight STS-93 revealed changes in the mRNA expression of roughly 5% of genes analyzed. These gene expression changes were compared with gene expression changes that occur during gravity perception and response in animal cells and multicellular plants. Our data contribute to a better understanding of the impact of space flight conditions, including microgravity, on cellular growth and development, and provide insights into the adaptive strategies of individual cells in response to these conditions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Abbreviations

1g :

1× Gravity earths gravitational force

OES:

Orbiter environmental simulator

Q RT-PCR:

Quantitative real-time reverse transcription PCR

BAGEL:

Bayesian analysis of gene expression level software

TUG:

Tentative unique gene

References

  1. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    PubMed  Article  CAS  Google Scholar 

  2. Blancaflor EB (2002) The cytoskeleton and gravitropism in higher plants. J Plant Growth Regul 21:120–136

    PubMed  Article  CAS  Google Scholar 

  3. Borner GHH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis A genomic analysis. Plant Physiol 129:486–499

    PubMed  Article  CAS  Google Scholar 

  4. Briarty LG, Maher EP (2004) Reserve utilization in seeds of Arabidopsis thaliana germinating in microgravity. Int J Plant Sci 165:545–551

    Article  Google Scholar 

  5. Bushart TJ, Roux SJ (2007) Conserved features of germination and polarized cell growth: a few insights from a pollen-fern spore comparison. Ann Bot (Lond) 99:9–17

    Article  CAS  Google Scholar 

  6. Cantero A, Barthakur S, Bushart TJ, Chou S, Morgan RO, Fernandez MP, Clark GB, Roux SJ (2006) Expression profiling of the Arabidopsis annexin gene family during germination, de-etiolation and abiotic stress. Plant Physiol Biochem 44:13–24

    PubMed  Article  CAS  Google Scholar 

  7. Chatterjee A, Porterfield DM, Smith PS, Roux SJ (2000) Gravity-directed calcium current in germinating spores of Ceratopteris richardii. Planta 210:607–610

    PubMed  Article  CAS  Google Scholar 

  8. Chow B, McCourt P (2006) Plant hormone receptors: perception is everything. Genes Dev 20:1998–2008

    PubMed  Article  CAS  Google Scholar 

  9. Cubano LA, Lewis ML (2001) Effect of vibrational stress and spaceflight on regulation of heat shock proteins hsp70 and hsp27 in human lymphocytes (Jurkat). J Leukocyte Biol 69:755–761

    PubMed  CAS  Google Scholar 

  10. Demaggio AE, Stetler DA (1980) Storage products in spores of Onoclea sensibilis L. Am J Bot 67:452–455

    Article  Google Scholar 

  11. Edwards ES, Roux SJ (1994) Limited period of graviresponsiveness in germinating spores of Ceratopteris richardi. Planta 195:150–152

    PubMed  Article  CAS  Google Scholar 

  12. Edwards ES, Roux SJ (1998) Influence of gravity and light on the developmental polarity of Ceratopteris richardii fern spores. Planta 205:553–560

    PubMed  Article  CAS  Google Scholar 

  13. Fasano JM, Swanson SJ, Blancaflor EB, Dowd PE, Kao TH, Gilroy S (2001) Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13:907–921

    PubMed  Article  CAS  Google Scholar 

  14. Fischer U, Men S, Grebe M (2004) Lipid function in plant cell polarity. Curr Opin Plant Biol 7:670–676

    PubMed  Article  CAS  Google Scholar 

  15. Hammond TG, Benes E, O’Reilly KC, Wolf DA, Linnehan RM, Taher A, Kaysen JH, Allen PL, Goodwin TJ (2000) Mechanical culture conditions effect gene expression: gravity-induced changes on the space shuttle. Physiol Genomics 3:163–173

    PubMed  CAS  Google Scholar 

  16. Hughes-Fulford M, Tjandrawinata R, Fitzgerald J, Gasuad K, Gilbertson V (1998) Effects of microgravity on osteoblast growth. Gravit Space Biol Bull 11:51–60

    PubMed  CAS  Google Scholar 

  17. Ikemoto M, Nikawa T, Takeda S, Watanabe C, Kitano T, Baldwin KM, Izumi R, Nonaka I, Towatari T, Teshima S, Rokutan K, Kishi K (2001) Space shuttle flight (STS-90) enhances degradation of rat myosin heavy chain in association with activation of ubiquitin-proteasome pathway. FASEB J 15:1279–1281

    PubMed  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  19. Kordyum EL (2003) Calcium signaling in plant cells in altered gravity. Adv Space Res 32:1621–1630

    PubMed  Article  CAS  Google Scholar 

  20. Kumei Y, Morita S, Nakamura H, Akiyama H, Hirano M, Shimokawa H, Ohya K (2003) Coinduction of GTP cyclohdyolase I and inducible NO synthase in rat osteoblasts during space flight: apoptotic and self-protective stress response? Ann NY Acad Sci 1010:481–485

    PubMed  Article  CAS  Google Scholar 

  21. Leung J, Orfanidi S, Chefdor F, Meszaros T, Bolte S, Mizoguchi T, Shinozaki K, Giraudat J, Bogre L (2006) Antagonistic interaction between MAP kinase and protein phosphatase 2C in stress recovery. Plant Sci 171:596–606

    Article  CAS  Google Scholar 

  22. Mahalingam R, Fedoroff N (2003) Stress response, cell death and signalling: the many faces of reactive oxygen species. Physiol Plant 119:56–68

    Article  CAS  Google Scholar 

  23. Mansfield SG, Briarty LG (1996) The dynamics of seedling and cotyledon cell development in Arabidopsis thaliana during reserve mobilization. Int J Plant Sci 157:280–295

    Article  Google Scholar 

  24. Moseyko N, Zhu T, Chang HS, Wang X, Feldman LJ (2002) Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe microarrays. Plant Physiol 130:720–728

    PubMed  Article  CAS  Google Scholar 

  25. Neuteboom LW, Ng JMY, Kuyper M, Clijdesdale OR, Hooykaas PJJ, van der Zaal BJ (1999) Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol 39:273–287

    PubMed  Article  CAS  Google Scholar 

  26. Papdi C, Abraham E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147:528–542

    PubMed  Article  CAS  Google Scholar 

  27. Paul A-L, Ferl RJ (2002) Molecular aspects of stress-gene regulation during spaceflight. J Plant Growth Regul 21:166–176

    PubMed  Article  CAS  Google Scholar 

  28. Paul A-L, Popp MP, Gurley WB, Guy C, Norwood KL, Ferl RJ (2005) Arabidopsis gene expression patterns are altered during spaceflight. Adv Space Res 36:1175–1181

    Article  Google Scholar 

  29. Pfeiffer I, Kutschera U (1997) Effect of white light on cell expansion and lipid metabolism in sunflower cotyledons. J Plant Physiol 151:590–594

    CAS  Google Scholar 

  30. Reyes D, Rodriguez D, Nicolas G, Nicolas C (2006) Evidence of a role for tyrosine dephosphorylation in the control of postgermination arrest of development by abscisic acid in Arabidopsis thaliana L. Planta 223:381–385

    PubMed  Article  CAS  Google Scholar 

  31. Roux SJ, Chatterjee A, Hillier S, Cannon T (2003) Early development of fern gametophytes in microgravity. Adv Space Res 31:215–220

    PubMed  Article  Google Scholar 

  32. Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol 141:1389–1399

    PubMed  Article  CAS  Google Scholar 

  33. Salmi ML, Bushart TJ, Stout SC, Roux SJ (2005) Profile and analysis of gene expression changes during early development in germinating spores of Ceratopteris richardii. Plant Physiol 138:1734–1745

    PubMed  Article  CAS  Google Scholar 

  34. Scott AC, Allen NS (1999) Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol 121:1291–1298

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  36. Townsend JP, Hartl D (2002) Bayesian analysis of gene expression levels: statistical quantification of relative mRNA level across multiple strains or treatments. Genome Biol 3:research0071.0071–research0071.0016

    Google Scholar 

Download references

Acknowledgments

We first thank Mr. William McLamb and Dr. David Chapman at Kennedy Space Center, whose experience and assistance were essential for the successful execution of the experiments. At the University of Texas we thank Mr. Thomas Bushart for expertise and assistance with Q RT-PCR, Dr. Jennifer Moon and Ms. Julia Kays for critical review of and helpful suggestions on the manuscript, and Dr. Vishy Iyer and these members of his laboratory for the use of his microarray equipment and for assistance and guidance in all aspects of microarray analysis: Dr. Jonghwan Kim, Mr. Jonathan Davies, Ms. Kerri Jeffers, and Ms. Xuan Lu, and Mr. Patrick Killion. This work was supported by NASA grants NAG2-1586 and NAG10-295 to S.J.R.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Stanley J. Roux.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental data (DOC 91 kb)

Supplemental data (XLS 112 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Salmi, M.L., Roux, S.J. Gene expression changes induced by space flight in single-cells of the fern Ceratopteris richardii . Planta 229, 151–159 (2008). https://doi.org/10.1007/s00425-008-0817-y

Download citation

Keywords

  • Space flight
  • Gravity
  • Gene expression
  • Microarray
  • Fern
  • Quantitative real-time RT-PCR