Organ-specific remodeling of the Arabidopsis transcriptome in response to spaceflight

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Paul, Anna Lisa ^a   Zupanska, Agata K ^a   Schultz, Eric R ^a   Ferl, Robert J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; ECOSYSTEM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SPACE FLIGHT; SPECIES DIFFERENCE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ECOSYSTEM; GENE EXPRESSION REGULATION, PLANT; SPACE FLIGHT; SPECIES SPECIFICITY; TRANSCRIPTOME;

EID: 84881038442     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-112     Document Type: Article

References (64)

1. Ferl RJ, Zupanska A, Spinale A, Reed D, Manning-Roach S, Guerra G, Cox DR, Paul A-L. The performance of KSC Fixation Tubes with RNALater for orbital experiments: A case study in ISS operations for molecular biology. Adv Space Res 2011, 48(1):199-206.
2. McLamb W, Wells HW. Passive cryogenic hardware for international space station flight experiments. SAE International 2003, SAE Technical Paper 2003-01-2526,.
3. Honma Y, Nakabayashi I, Tamaoki D, Kasahara H, Ishioka N, Shimazu T, Yamada M, Karahara I, Kamisaka S. Optical microscopy of Arabidopsis seedlings fixed in non-fresh FAA using Kennedy fixation tubes. Biol Sci Space 2003, 17(4):307-308. 10.2187/bss.17.307, 15136754.
4. Decadal-Survey-Commitee The Decadal Survey on Biological and Physical Sciences in Space - National Research Council: Recapturing a Future for Space Exploration: Life and Physical Sciences Research for a New Era 2011, 63-66. Council NR: The National Academies Press, http://www.nap.edu/catalog.php?record_id=13048, Decadal-Survey-Commitee.
5. Ričkienė A. Space plant biology research in Lithuania. Endeavour 2012, 36(3):117-124. 10.1016/j.endeavour.2012.04.002, 22613222.
6. Wolverton C, Kiss JZ. An update on plant space biology. Gravitational Space Biol 2009, 22:13-20.
7. Wyatt SE, Kiss JZ. Plant tropisms: from Darwin to the international space station. Am J Bot 2013, 100(1):1-3. 10.3732/ajb.1200591, 23281390.
8. Dayanandan P. Gravitational biology and space life sciences: current status and implications for the Indian space programme. J Biosci 2011, 36(5):911-919. 10.1007/s12038-011-9150-x, 22116289.
9. Paul A-L, Wheeler RM, Levine HG, Ferl RJ. Fundamental plant biology enabled by The Space Shuttle. Am J Bot 2013, 100(1):226-234. 10.3732/ajb.1200338, 23281389.
10. Wolff SA, Coelho LH, Zabrodina M, Brinckmann E, Kittang A-I. Plant mineral nutrition, gas exchange and photosynthesis in space: a review. Adv Space Res 2013, 51:465-475.
11. Edwards W, Moles A. Re-contemplate an entangled bank: the power of movement in plants revisited. Bot J Linn Soc 2009, 160:111-118.
12. Stout SC, Porterfield DM, Briarty LG, Kuang A, Musgrave ME. Evidence of root zone hypoxia in Brassica rapa L. grown in microgravity. Int J Plant Sci 2001, 162(2):249-255. 10.1086/319585, 11725801.
13. Brinckmann E. ESA hardware for plant research on the international space station. Adv Space Res 2005, 36(7):1162-1166.
14. Zupanska AK, Denison FC, Ferl RJ, Paul A-L. Spaceflight engages heat shock protein and other molecular chaperone genes in tissue culture cells of Arabidopsis thaliana. Am J Bot 2013, 100(1):235-248. 10.3732/ajb.1200343, 23258370.
15. Paul A-L, Popp MP, Gurley WB, Guy CL, Norwood KL, Ferl RJ. Arabidopsis gene expression patterns are altered during spaceflight. Adv Space Res 2005, 36(7):1175-1181.
16. Paul A-L, Zupanska A, Ostrow DT, Zhang Y, Sun Y, Li J-L, Shanker S, Farmerie WG, Amalfitano CE, Ferl RJ. Spaceflight transcriptomes: unique responses to a novel environment. Astrobiology 2012, 12:40-56. 10.1089/ast.2011.0696, 3264962, 22221117.
17. Salmi ML, Bushart TJ, Roux SJ. Autonomous gravity perception and responses of single plant cells. Gravitational Space Biol 2011, 25(1):6-13.
18. Salmi ML, Roux SJ. Gene expression changes induced by space flight in single-cells of the fern Ceratopteris richardii. Planta 2008, 229(1):151-159. 10.1007/s00425-008-0817-y, 18807069.
19. Stutte GW, Monje O, Hatfield RD, Paul AL, Ferl RJ, Simone CG. Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat. Planta 2006, 224(5):1038-1049. 10.1007/s00425-006-0290-4, 16708225.
20. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95(25):14863-14868. 10.1073/pnas.95.25.14863, 24541, 9843981.
21. Millar KD, Kumar P, Correll MJ, Mullen JL, Hangarter RP, Edelmann RE, Kiss JZ. A novel phototropic response to red light is revealed in microgravity. New Phytol 2010, 186(3):648-656. 10.1111/j.1469-8137.2010.03211.x, 20298479.
22. Solheim BG, Johnsson A, Iversen TH. Ultradian rhythms in Arabidopsis thaliana leaves in microgravity. New Phytol 2009, 183(4):1043-1052. 10.1111/j.1469-8137.2009.02896.x, 19538548.
23. Iversen TH, Fossum KR, Svare H, Johnsson A, Schiller P. Plant growth using EMCS hardware on the ISS. J Gravit Physiol 2002, 9(1):P223-224.
24. Häuplik-Meusburger S, Peldszus R, Holzgethan V. Greenhouse design integration benefits for extended spaceflight. Acta Astronaut 2011, 68(1):85-90.
25. Wheeler RM. Plants for human life support in space: From Myers to Mars. Gravitational Space Biol 2010, 23:25-35.
26. Drysdale AE, Ewert MK, Hanford AJ. Life support approaches for Mars missions. Adv Space Res 2003, 31(1):51-61. 10.1016/S0273-1177(02)00658-0, 12577926.
27. Spalding EP. Diverting the downhill flow of auxin to steer growth during tropisms. Am J Bot 2013, 100(1):203-214. 10.3732/ajb.1200420, 23284058.
28. Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. Molecular basis of the core regulatory network in aba responses: sensing, signaling and transport. Plant Cell Physiol 2010, 51(11):1821-1839. 10.1093/pcp/pcq156, 2978318, 20980270.
29. Benatti MR, Penning BW, Carpita NC, McCann MC. We are good to grow: dynamic integration of cell wall architecture with the machinery of growth. Front Plant Sci 2012, 3:187. 3424494, 22936938.
30. Chapman EJ, Greenham K, Castillejo C, Sartor R, Bialy A, Sun TP, Estelle M. Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS One 2012, 7(5):e36210. 10.1371/journal.pone.0036210, 3348943, 22590525.
31. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J. Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 2000, 277:305-310. 10.1006/bbrc.2000.3672, 11032722.
32. Ozawa R, Arimura G, Takabayashi J, Shimoda T, Nishioka T. Involvement of jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiol 2000, 41(4):391-398. 10.1093/pcp/41.4.391, 10845451.
33. Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T. Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development 2004, 131(5):1089-1100. 10.1242/dev.00925, 14973283.
34. Baldwin KL, Strohm AK, Masson PH. Gravity sensing and signal transduction in vascular plant primary roots. Am J Bot 2013, 100(1):126-142. 10.3732/ajb.1200318, 23048015.
35. Matsuda S, Kajizuka T, Kadota A, Nishimura T, Koshiba T. NPH3- and PGP-like genes are exclusively expressed in the apical tip region essential for blue-light perception and lateral auxin transport in maize coleoptiles. J Exp Bot 2011, 62(10):3459-3466. 10.1093/jxb/err019, 3130171, 21459767.
36. Refregier G, Pelletier S, Jaillard D, Hofte H. Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol 2004, 135(2):959-968. 10.1104/pp.104.038711, 514130, 15181211.
37. Gimeno-Gilles C, Lelievre E, Viau L, Malik-Ghulam M, Ricoult C, Niebel A, Leduc N, Limami AM. ABA-mediated inhibition of germination is related to the inhibition of genes encoding cell-wall biosynthetic and architecture: modifying enzymes and structural proteins in Medicago truncatula embryo axis. Mol Plant 2009, 2(1):108-119. 10.1093/mp/ssn092, 2639729, 19529818.
38. Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 2004, 134(4):1555-1573. 10.1104/pp.103.034736, 419831, 15047898.
39. Paul A-L, Amalfitano CE, Ferl RJ. Plant growth strategies are remodeled by spaceflight. BMC Plant Biol 2012, 12(1):232. 10.1186/1471-2229-12-232, 3556330, 23217113.
40. Nibau C, Gibbs DJ, Bunting KA, Moody LA, Smiles EJ, Tubby JA, Bradshaw SJ, Coates JC. ARABIDILLO proteins have a novel and conserved domain structure important for the regulation of their stability. Plant MolBiol 2011, 75(1-2):77-92.
41. Walley JW, Kelley DR, Nestorova G, Hirschberg DL, Dehesh K. Arabidopsis deadenylases AtCAF1a and AtCAF1b play overlapping and distinct roles in mediating environmental stress responses. Plant Physiol 2010, 152(2):866-875. 10.1104/pp.109.149005, 2815882, 19955262.
42. Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. The Plant cell 1995, 7(10):1555-1567. 161010, 7580251.
43. Bosch M, Mayer CD, Cookson A, Donnison IS. Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. J Exp Bot 2011, 62(10):3545-3561. 10.1093/jxb/err045, 3130177, 21402660.
44. Lamport DT, Kieliszewski MJ, Chen Y, Cannon MC. Role of the extensin superfamily in primary cell wall architecture. Plant Physiol 2011, 156(1):11-19. 10.1104/pp.110.169011, 3091064, 21415277.
45. Bohme K, Li Y, Charlot F, Grierson C, Marrocco K, Okada K, Laloue M, Nogue F. The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. Plant J 2004, 40(5):686-698. 10.1111/j.1365-313X.2004.02245.x, 15546352.
46. Yoo CM, Quan L, Cannon AE, Wen J, Blancaflor EB. AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J 2012, 69(6):1064-1076. 10.1111/j.1365-313X.2011.04856.x, 22098134.
47. Sibout R, Sukumar P, Hettiarachchi C, Holm M, Muday GK, Hardtke CS. Opposite root growth phenotypes of hy5 versus hy5 hyh mutants correlate with increased constitutive auxin signaling. PLoS Genet 2006, 2(11):e202. 10.1371/journal.pgen.0020202, 1657057, 17121469.
48. Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 2007, 19(3):731-749. 10.1105/tpc.106.047688, 1867377, 17337630.
49. Toyota M, Gilroy S. Gravitropism and mechanical signaling in plants. Am J Bot 2013, 100(1):111-125. 10.3732/ajb.1200408, 23281392.
50. Hohm T, Preuten T, Fankhauser C. Phototropism: translating light into directional growth. Am J Bot 2013, 100(1):47-59. 10.3732/ajb.1200299, 23152332.
51. Cassab GI, Eapen D, Campos ME. Root hydrotropism: an update. Am J Bot 2013, 100(1):14-24. 10.3732/ajb.1200306, 23258371.
52. Blancaflor EB. Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am J Bot 2013, 100(1):143-152. 10.3732/ajb.1200283, 23002165.
53. Millar KD, Johnson CM, Edelmann RE, Kiss JZ. An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 2011, 11(8):787-797. 10.1089/ast.2011.0699, 3233217, 21970704.
54. Kiss JZ, Millar KD, Edelmann RE. Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station. Planta 2012, 236:635-645. 10.1007/s00425-012-1633-y, 22481136.
55. Salmi ML, uL Haque A, Bushart TJ, Stout SC, Roux SJ, Porterfield DM. Changes in gravity rapidly alter the magnitude and direction of a cellular calcium current. Planta 2011, 233(5):911-920. 10.1007/s00425-010-1343-2, 21234599.
56. Paul A-L, Schuerger AC, Popp MP, Richards JT, Manak MS, Ferl RJ. Hypobaric biology: Arabidopsis gene expression at low atmospheric pressure. Plant Physiol 2004, 134(1):215-223. 10.1104/pp.103.032607, 316301, 14701916.
57. Sheen J, Hwang S, Niwa Y, Kobayashi H, Galbraith DW. Green-fluorescent protein as a new vital marker in plant cells. Plant J 1995, 8(5):777-784. 10.1046/j.1365-313X.1995.08050777.x, 8528289.
58. Manak MS, Paul AL, Sehnke PC, Ferl RJ. Remote sensing of gene expression in Planta: transgenic plants as monitors of exogenous stress perception in extraterrestrial environments. Life Support Biosph Sci 2002, 8(2):83-91.
59. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 1997, 9(11):1963-1971. 157050, 9401121.
60. Advanced Biological Research System (ABRS) http://www.nasa.gov/mission_pages/station/research/experiments/ABRS.html.
61. Transgenic Arabidopsis Gene Expression System (TAGES) http://www.nasa.gov/mission_pages/station/research/experiments/TAGES.html.
62. Paul A-L, Murdoch T, Ferl E, Levine HG, Ferl RJ. The TAGES imaging system: Optimizing a green fluorescent protein imaging system for plants. SAE International 2003, SAE Technical Paper 2003-01-2477.
63. Collins TJ. ImageJ for microscopy. Biotechniques 2007, 43(1 Suppl):25-30.
64. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000, 25(2):169-193. 10.1677/jme.0.0250169, 11013345.