Parabolic flight induces changes in gene expression patterns in arabidopsis thaliana

Astrobiology

Volumn 11, Issue 8, 2011, Pages 743-758

  Paul, Anna Lisa ^a   Manak, Michael S ^a,b   Mayfield, John D ^a,c   Reyes, Matthew F ^a,d   Gurley, William B ^a   Ferl, Robert J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DUKE UNIVERSITY   (United States)

^d Exploration Solutions Inc   (United States)

Author keywords

Microarray; Microgravity; NASA Reduced Gravity Office; Signal transduction; Spaceflight analogue; Transcriptome

Indexed keywords

ARABIDOPSIS PROTEIN; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT GENOME; SIGNAL TRANSDUCTION; SPACE FLIGHT; WEIGHTLESSNESS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; SIGNAL TRANSDUCTION; SPACE FLIGHT; TRANSCRIPTOME; WEIGHTLESSNESS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 80054866558     PISSN: 15311074     EISSN: None     Source Type: Journal    
DOI: 10.1089/ast.2011.0659     Document Type: Article

References (88)

1. Barnes, S.A., Quaggio, R.B., and Chua, N.H. (1995) Phytochrome signal-transduction: characterization of pathways and isolation of mutants. Philos Trans R Soc Lond B Biol Sci 350:67-74.
2. Benjamins, R., Ampudia, C.S., Hooykaas, P.J., and Offringa, R. (2003) PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol 132:1623-1630. (Pubitemid 36872909)
3. Bishopp, A., Benkova, E., and Helariutta, Y. (2010) Sending mixed messages: auxin-cytokinin crosstalk in roots. Curr Opin Plant Biol 14:10-16.
4. Blancaflor, E.B. and Masson, P.H. (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol 133:1677-1690. (Pubitemid 38047299)
5. Boudsocq, M., Willmann, M.R., McCormack, M., Lee, H., Shan, L., He, P., Bush, J., Cheng, S.H., and Sheen, J. (2010) Differential innate immune signalling via Ca(2 +) sensor protein kinases. Nature 464:418-422.
6. Bucker, H., Horneck, G., Allkofer, O.C., Bartholoma, K.P., Beaujean, R., Cuer, P., Enge, W., Facius, R., Francois, H., Graul, E.H. Henig, G., Heinrich, W., Kaiser, R., Kuhn, H., Massue, J.P., Planel, H., Portal, G., Reinholz, E., Ruther, W., Scheuermann, W., Schmitt, R., Schopper, E., Schott, J.U., So-leilhavoup, J.P., and Wollenhaupt, H. (1973) The Biostack experiment on Apollo 16. Life Sci Space Res 11:295-305.
7. Bustin, S.A. (2000) Absolute quantification of mRNA using realtime reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169-193.
8. Chatterjee, A., Porterfield, D.M., Smith, P.S., and Roux, S.J. (2000) Gravity-directed calcium current in germinating spores of Ceratopteris richardii. Planta 210:607-610. (Pubitemid 30192173)
9. Darwin, C. and Darwin, F. (1881) The Power of Movement in Plants, John Murray, London.
10. Diaz, J. and Alvarez-Buylla, E.R. (2006) A model of the ethylene signaling pathway and its gene response in Arabidopsis thali-ana: pathway cross-talk and noise-filtering properties. Chaos 16:023112.
11. Dreschel, T.W., Brown, C.S., Piastuch, W.C., Hinkle, C.R., and Knott, W.M. (1994) Porous tube plant nutrient delivery system development: a device for nutrient delivery in microgravity. Adv Space Res 14:47-51.
12. Du, L., Ali, G.S., Simons, K.A., Hou, J., Yang, T., Reddy, A.S., and Poovaiah, B.W. (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154-1158.
13. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868. (Pubitemid 29003722)
14. Fasano, J.M., Massa, G.D., and Gilroy, S. (2002) Ionic signaling in plant responses to gravity and touch. J Plant Growth Regul 21:71-88. (Pubitemid 34788823)
15. Friml, J., Benkova, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jü rgens, G., and Palme, K. (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661-673. (Pubitemid 34241427)
16. Gilroy, S. (2008) Plant tropisms. Curr Biol 18:R275-R277. (Pubitemid 351458694)
17. Guikema, J.A., DeBell, L., Paulsen, A., Spooner, B.S., and Wong, P.P. (1994) Clover development during spaceflight: a model system. Adv Space Res 14:173-176.
18. Guilfoyle, T.J. and Hagen, G. (2007) Auxin response factors. Curr Opin Plant Biol 10:453-460. (Pubitemid 47505406)
19. Hashemi, B.B., Penkala, J.E., Vens, C., Huls, H., Cubbage, M., and Sams, C.F. (1999) T cell activation responses are differentially regulated during clinorotation and in spaceflight. FASEB J 13:2071-2082. (Pubitemid 29517637)
20. Hatton, J.P., Gaubert, F., Lewis, M.L., Darsel, Y., Ohlmann, P., Cazenave, J.P., and Schmitt, D. (1999) The kinetics of translocation and cellular quantity of protein kinase C in human leukocytes are modified during spaceflight. FASEB J 13:S23-S33.
21. Hong-Bo, S., Li-Ye, C., and Ming-An, S. (2008) Calcium as a versatile plant signal transducer under soil water stress. Bioessays 30:634-641. (Pubitemid 351898013)
22. Hoshino, T., Hitotsubashi, R., Miyamoto, K., Tanimoto, E., and Ueda, J. (2003) Expression of PIN and AUX1 genes encoding putative carrier proteins for auxin polar transport in etiolated pea epicotyls under simulated microgravity conditions on a three-dimensional clinostat. Biol Sci Space 17:175-176.
23. Hughes-Fulford, M. (2001) Changes in gene expression and signal transduction in microgravity. J Gravit Physiol 8:P1-P4.
24. Hughes-Fulford, M. (2002) The role of signaling pathways in osteoblast gravity perception. J Gravit Physiol 9:P257-P260.
25. Johnson, C.F., Dreschel, T.W., Brown, C.S., and Wheeler, R.M. (1996) Optimization of moisture content for wheat seedling germination in a cellulose acetate medium for a space flight experiment. Adv Space Res 18:239-242.
26. Jonsson, H., Heisler, M.G., Shapiro, B.E., Meyerowitz, E.M., and Mjolsness, E. (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103:1633-1638. (Pubitemid 43191216)
27. Kamada, M., Fujii, N., Aizawa, S., Kamigaichi, S., Mukai, C., Shimazu, T., and Takahashi, H. (2000) Control of grav-imorphogenesis by auxin: accumulation pattern of CS-IAA1 mRNA in cucumber seedlings grown in space and on the ground. Planta 211:493-501.
28. Kanchiswamy, C.N., Takahashi, H., Quadro, S., Maffei, M.E., Bossi, S., Bertea, C., Zebelo, S.A., Muroi, A., Ishihama, N., Yoshioka, H., Boland, W., Takabayashi, J., Endo, Y., Sawasaki, T., and Arimura, G. (2010) Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol 10:97.
29. Kaseda, R., Iino, N., Hosojima, M., Takeda, T., Hosaka, K., Ko-bayashi, A., Yamamoto, K., Suzuki, A., Kasai, A., Suzuki, Y., Gejyo, F., and Saito, A. (2007) Megalin-mediated endocytosis of cystatin C in proximal tubule cells. Biochem Biophys Res Commun 357:1130-1134. (Pubitemid 46693689)
30. Kepinski, S. (2007) The anatomy of auxin perception. Bioessays 29:953-956. (Pubitemid 47522835)
31. Kerr, I.D. and Bennett, M.J. (2007) New insight into the biochemical mechanisms regulating auxin transport in plants. Biochem J 401:613-622. (Pubitemid 46219255)
32. Kimbrough, J.M., Salinas-Mondragon, R., Boss, W.F., Brown, C.S., and Sederoff, H.W. (2004) The fast and transient tran-scriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 136:2790-2805.
33. Kitaya, Y., Kawai, M., Tsuruyama, J., Takahashi, H., Tani, A., Goto, E., Saito, T., and Kiyota, M. (2001) The effect of gravity on surface temperature and net photosynthetic rate of plant leaves. Adv Space Res 28:659-664. (Pubitemid 34002369)
34. Kitaya, Y., Kawai, M., Tsuruyama, J., Takahashi, H., Tani, A., Goto, E., Saito, T., and Kiyota, M. (2003) The effect of gravity on surface temperatures of plant leaves. Plant Cell Environ 26:497-503. (Pubitemid 36521856)
35. Lanteri, M.L., Pagnussat, G.C., and Lamattina, L. (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide-and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341-1351.
36. Li,Y., Dai, X., Cheng, Y., and Zhao, Y. (2011) NPY genes play an essential role in root gravitropic responses in Arabidopsis. Mol Plant 4:171-179.
37. 2 bioavailability in microgravity. Adv Space Res 34:1579-1584.
38. Llorente, F., Muskett, P., Sanchez-Vallet, A., Lopez, G., Ramos, B., Sanchez-Rodriguez, C., Jorda, L., Parker, J., and Molina, A. (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant 1:496-509.
39. Lomax, T.L. (1997) Molecular genetic analysis of plant gravi-tropism. Gravit Space Biol Bull 10:75-82.
40. Luschnig, C., Gaxiola, R.A., Grisafi, P., and Fink, G.R. (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175-2187. (Pubitemid 28348041)
41. Ma, S. and Bohnert, H.J. (2007) Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 8:R49.
42. Martzivanou, M., Babbick, M., Cogoli-Greuter, M., and Hampp, R. (2006) Microgravity-related changes in gene expression after short-term exposure of Arabidopsis thaliana cell cultures. Protoplasma 229:155-162. (Pubitemid 44974251)
43. Miyamoto, K., Hoshino, T., Hitotsubashi, R., Tanimoto, E., and Ueda, J. (2003) Graviresponse and its regulation from the aspect of molecular levels in higher plants: growth and development, and auxin polar transport in etiolated pea seedlings under microgravity. Biol Sci Space 17:234-235.
44. Miyamoto, K., Hoshino, T., Yamashita, M., and Ueda, J. (2005) Automorphosis of etiolated pea seedlings in space is simulated by a three-dimensional clinostat and the application of inhibitors of auxin polar transport. Physiol Plant 123:467-474. (Pubitemid 40534314)
45. Moreno-Risueno, M.A., Van Norman, J.M., Moreno, A., Zhang, J., Ahnert, S.E., and Benfey, P.N. (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306-1311.
46. Morita, M.T. and Tasaka, M. (2004) Gravity sensing and signaling. Curr Opin Plant Biol 7:712-718. (Pubitemid 39379515)
47. Moseyko, N. and Feldman, L.J. (2002) VIZARD: analysis of Af-fymetrix Arabidopsis GeneChip data. Bioinformatics 18:1264-1265.
48. Moseyko, N., Zhu, T., Chang, H.S., Wang, X., and Feldman, L.J. (2002) Transcription profiling of the early gravitropic response in Arabidopsis using high-density oligonucleotide probe mi-croarrays. Plant Physiol 130:720-728. (Pubitemid 35224779)
49. Moubayidin, L., Di Mambro, R., and Sabatini, S. (2009) Cytoki-nin-auxin crosstalk. Trends Plant Sci 14:557-562.
50. Norikane, J.H., Jones, S.B., Steinberg, S.L., Levine, H.G., and Or. D. (2005) Porous media matric potential and water content measurements during parabolic flight. Habitation (Elmsford) 10:117-126.
51. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., and Tasaka, M. (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118-130. (Pubitemid 46852706)
52. Palme, K., Dovzhenko, A., and Ditengou, F.A. (2006) Auxin transport and gravitational research: perspectives. Protoplasma 229:175-181. (Pubitemid 44974253)
53. Paponov, I.A., Teale, W.D., Trebar, M., Blilou, I., and Palme, K. (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170-177. (Pubitemid 40466204)
54. Paul, A.L., Daugherty, C.J., Bihn, E.A., Chapman, D.K., Norwood, K.L., and Ferl, R.J. (2001) Transgene expression patterns indicate that spaceflight affects stress signal perception and transduction in arabidopsis. Plant Physiol 126:613-621. (Pubitemid 32566616)
55. Paul, A.L., Schuerger, A.C., Popp, M.P., Richards, J.T., Manak, M.S., and Ferl, R.J. (2004) Hypobaric biology: Arabidopsis gene expression at low atmospheric pressure. Plant Physiol 134:215-223. (Pubitemid 38178694)
56. Paul, A.L., Popp, M.P., Gurley, W.B., Guy, C., Norwood, K.L., and Ferl, R. (2005) Arabidopsis gene expression patterns are altered during spaceflight. Adv Space Res 36:1175-1181. (Pubitemid 41642060)
57. Perbal, G. and Driss-Ecole, D. (2003) Mechanotransduction in gravisensing cells. Trends Plant Sci 8:498-504. (Pubitemid 37325560)
58. Perera, I.Y., Heilmann, I., Chang, S.C., Boss, W.F., and Kaufman, P.B. (2001) A role for inositol 1,4,5-trisphosphate in gravitropic signaling and the retention of cold-perceived gravistimulation of oat shoot pulvini. Plant Physiol 125:1499-1507. (Pubitemid 32224637)
59. Perrin, R.M., Young, L.S., Murthy, U.M.N., Harrison, B.R., Wang, Y., Will, J.L., and Masson, P.H. (2005) Gravity signal transduction in primary roots. Ann Bot 96:737-743. (Pubitemid 41330543)
60. Perrot-Rechenmann, C. (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2, doi:10.1101/cshperspect.a001446.
61. Plieth, C. (2005) Calcium: just another regulator in the machinery of life? Ann Bot 96:1-8. (Pubitemid 41389590)
62. Poovaiah, B.W., Yang, T., and van Loon, J.J. (2002) Calcium/calmodulin- mediated gravitropic response in plants. J Gravit Physiol 9:P211-P214.
63. Porterfield, D.M. (2002) The biophysical limitations in physiological transport and exchange in plants grown in micro-gravity. J Plant Growth Regul 21:177-190. (Pubitemid 34788832)
64. Price, A.H., Taylor, A., Ripley, S.J., Griffiths, A., Trewavas, A.J., and Knight, M.R. (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301-1310.
65. Reddi, L.N., Xiao, M., and Steinberg, S.L. (2005) Discontinuous pore fluid distribution under microgravity-KC-135 flight investigations. Soil Sci Soc Am J 69:593-598. (Pubitemid 40660517)
66. Rentel, M.C. and Knight, M.R. (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135:1471-1479. (Pubitemid 39009393)
67. Rosen, E., Chen, R., and Masson, P.H. (1999) Root gravitropism: a complex response to a simple stimulus? Trends Plant Sci 4:407-412. (Pubitemid 29471624)
68. Shiina, T., Nishii, A., Toyoshima, Y., and Bogorad, L. (1997) Identification of promoter elements involved in the cytosolic Ca(2+)-mediated photoregulation of maize cab-m1 expression. Plant Physiol 115:477-483. (Pubitemid 28395295)
69. Shimazu, T., Yuda, T., Miyamoto, K., Yamashita, M., and Ueda, J. (2001) Growth and development in higher plants under simulated microgravity conditions on a 3-dimensional clino-stat. Adv Space Res 27:995-1000. (Pubitemid 32792922)
70. Sieberer, T., Seifert, G.J., Hauser, M.T., Grisafi, P., Fink, G.R., and Luschnig, C. (2000) Post-transcriptional control of the Arabi-dopsis auxin efflux carrier EIR1 requires AXR1. Curr Biol 10:1595-1598. (Pubitemid 32062662)
71. Simon, P. (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439-1440. (Pubitemid 36939825)
72. Son, O., Hur, Y.S., Kim, Y.K., Lee, H.J., Kim, S., Kim, M.R., Nam, K.H., Lee, M.S., Kim, B.Y., Park, J., Park, J., Lee, S.C., Hanada, A., Yamaguchi, S., Lee, I.J., Kim, S.K., Yun, D.J., Söderman, E., and Cheon, C.I. (2010) ATHB12, an ABA-inducible home-odomain-leucine zipper (HD-Zip) protein of Arabidopsis, negatively regulates the growth of the inflorescence stem by decreasing the expression of a gibberellin 20-oxidase gene. Plant Cell Physiol 51:1537-1547.
73. Spoel, S.H. and Dong, X. (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3:348-351. (Pubitemid 351773103)
74. Stutte, G.W., Monje, O., Hatfield, R.D., Paul, A.L., Ferl, R.J., and Simone, C.G. (2006) Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat. Planta 224:1038-1049. (Pubitemid 44435855)
75. Swatzell, L.J. and Kiss, J.Z. (2000) Journey towards the centre of the Earth: plant gravitropism. Biologist (London) 47:229-233.
76. Taylor, W.E., Bhasin, S., Lalani, R., Datta, A., and Gonzalez-Cadavid, N.F. (2002) Alteration of gene expression profiles in skeletal muscle of rats exposed to microgravity during a spaceflight. J Gravit Physiol 9:61-70.
77. Toyota, M., Furuichi, T., Tatsumi, H., and Sokabe, M. (2008) Critical consideration on the relationship between auxin transport and calcium transients in gravity perception of Arabidopsis seedlings. Plant Signal Behav 3:521-524.
78. Tuteja, N. and Mahajan, S. (2007) Further characterization of calcineurin B-like protein and its interacting partner CBL-interacting protein kinase from Pisum sativum. Plant Signal Behav 2:358-361. (Pubitemid 350124657)
79. Ueda, J., Miyamoto, K., Yuda, T., Hoshino, T., Sato, K., Fujii, S., Kamigaichi, S., Izumi, R., Ishioka, N., Aizawa, S., Yoshizaki, I., Shimazu, T., and Fukui, K. (2000) STS-95 space experiment for plant growth and development, and auxin polar transport. Biol Sci Space 14:47-57.
80. Vadassery, J. and Oelmuller, R. (2009) Calcium signaling in pathogenic and beneficial plant microbe interactions: what can we learn from the interaction between Piriformospora indica and Arabidopsis thaliana. Plant Signal Behav 4:1024-1027.
81. Vanhaeren, H., Gonzalez, N., and Inzé, D. (2010) Hide and seek: uncloaking the vegetative shoot apex of Arabidopsis thaliana. Plant J 63:541-548.
82. Wang, S., Tiwari, S.B., Hagen, G., and Guilfoyle, T.J. (2005) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17:1979-1993.
83. Weijers, D., Sauer, M., Meurette, O., Friml, J., Ljung, K., Sand-berg, G., Hooykaas, P., and Offringa, R. (2005) Maintenance of embryonic auxin distribution for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis. Plant Cell 17:2517-2526.
84. Weinl, S. and Kudla, J. (2009) The CBL-CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytol 184:517-528.
85. Wolverton, C., Ishikawa, H., and Evans, M.L. (2002) The kinetics of root gravitropism: dual motors and sensors. J Plant Growth Regul 21:102-112. (Pubitemid 34788825)
86. Woodward, A.W. and Bartel, B. (2005) A receptor for auxin. Plant Cell 17:2425-2429.
87. Xiao, Y.H., Li, D.M., Yin, M.H., Li, X.B., Zhang, M., Wang, Y.J., Dong, J., Zhao, J., Luo, M., Luo, X.Y., Hou, L., Hu, L., and Pei, Y. (2010) Gibberellin 20-oxidase promotes initiation and elongation of cotton fibers by regulating gibberellin synthesis. J Plant Physiol 167:829-837.
88. Yamasaki, K., Kigawa, T., Inoue, M., Tateno, M., Yamasaki, T., Yabuki, T., Aoki, M., Seki, E., Matsuda, T., Tomo, Y., Hayami, N., Terada, T., Shirouzu, M., Osanai, T., Tanaka, A., Seki, M., Shinozaki, K., and Yokoyama, S. (2004) Solution structure of the B3 DNA binding domain of the Arabidopsis cold-responsive transcription factor RAV1. Plant Cell 16:3448-3459. (Pubitemid 41096018)