(Not) Keeping the stem straight: a proteomic analysis of maritime pine seedlings undergoing phototropism and gravitropism
Tóm tắt
Plants are subjected to continuous stimuli from the environment and have evolved an ability to respond through various growth and development processes. Phototropism and gravitropism responses enable the plant to reorient with regard to light and gravity. We quantified the speed of maritime pine seedlings to reorient with regard to light and gravity over 22 days. Seedlings were inclined at 15, 30 and 45 degrees with vertical plants as controls. A lateral light source illuminated the plants and stem movement over time was recorded. Depending on the initial angle of stem lean, the apical response to the lateral light source differed. In control and 15° inclined plants, the apex turned directly towards the light source after only 2 h. In plants inclined at 30° and 45°, the apex first reoriented in the vertical plane after 2 h, then turned towards the light source after 24 h. Two-dimensional gel electrophoresis coupled with mass spectrometry was then used to describe the molecular response of stem bending involved in photo- and gravi-tropism after 22 hr and 8 days of treatment. A total of 486 spots were quantitatively analyzed using image analysis software. Significant changes were determined in the protein accumulation of 68 protein spots. Early response gravitropic associated proteins were identified, which are known to function in energy related and primary metabolism. A group of thirty eight proteins were found to be involved in primary metabolism and energy related metabolic pathways. Degradation of Rubisco was implicated in some protein shifts. Our study demonstrates a rapid gravitropic response in apices of maritime pine seedlings inclined >30°. Little or no response was observed at the stem bases of the same plants. The primary gravitropic response is concomitant with a modification of the proteome, consisting of an over accumulation of energy and metabolism associated proteins, which may allow the stem to reorient rapidly after bending.
Tài liệu tham khảo
Farnsworth KD, Niklas KJ: Theories of optimization, form and function in branching architecture in plants. Functional Ecology. 1995, 9: 355-363. 10.2307/2389997.
Hart JW: Plant Tropisms and Other Growth Movements. London: Routledge, Chapman & Hall 1990.
Correll MJ, Kiss JZ: Interactions between gravitropism and phototropism in plants. Journal of Plant Growth Regulation. 2002, 21: 89-101. 10.1007/s003440010056.
Timell T: Compression wood in Gymniosperms. Heilderberg: Springer-Verlag 1986.
Knight T: On the direction of the radicle and germen during the vegetation of seeds. Philosophical Transactions of the Royal Society of London. 1806, 1: 99-108. 10.1098/rstl.1806.0006.
Fukaki H, Fujisawa H, Tasaka M: Gravitropic response of inflorescence stems in Arabidopsis thaliana. Plant Physiology. 1996, 110: 933-943. 10.1104/pp.110.3.933.
Hoson T, Kamisaka S, Masuda Y, Yamashita M: Changes in plant growth processes under microgravity conditions simulated by a three dimensional clinostat. Botanical Magazine. 1992, 105: 53-70. 10.1007/BF02489403.
Brown A, Dahl A, Chapman D: Morphology of Arabidopsis grown under chronic centrifugation and on the clinostat. Plant Physiology. 1976, 57: 338-364. 10.1104/pp.57.3.358.
Hoson T, Soga K, Mori R, Saiki M, Nakamura Y, Wakabayashi K, Kamisaka S: Cell wall changes involved in the automorphic curvature of rice coleoptiles under microgravity conditions in space. Journal of Plant Research. 2004, 117: 449-455. 10.1007/s10265-004-0182-2.
Kwon M, Bedgar D, Piastuch W, Davin L, Lewis N: Induced compression wood formation in Douglas fir (Pseudotsuga menziesii) in microgravity. Phytochemistry. 2001, 57: 847-857. 10.1016/S0031-9422(01)00145-5.
Volkmann D, Buchen B, Hejnowicz Z, Tewinkel M, Sievers A: Oriented movement of statoliths studied in a reduced gravitational-field during parabolic flights of rockets. Planta. 1991, 185: 153-161. 10.1007/BF00194056.
Fischer K, Schopfer P: Physical strain-mediated microtubule reorientation in the epidermis of gravitropically or phototropically stimulated maize coleoptiles. The Plant Journal. 1998, 15: 119-123. 10.1046/j.1365-313X.1998.00173.x.
Galland P: Tropisms of Avena coleoptiles: sine law for gravitropism, exponential law for photogravitropic equilibrium. Planta. 2002, 215: 779-784. 10.1007/s00425-002-0813-6.
Lariguet P, Fankhauser C: Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. The Plant Journal. 2004, 40: 826-834. 10.1111/j.1365-313X.2004.02256.x.
Zobel BJ, van Buijtenen JP: Wood Variation: Its Causes and Control. Heilderberg: Springer-Verlag 1989.
Vitha S, Zhao L, Sack F: Interaction of root gravitropism and phototropism in Arabidopsis wild type and starchless mutant. Plant Physiology. 2000, 122: 453-461. 10.1104/pp.122.2.453.
Matsuzaki J, Masumori M, Tange T: Phototropic bending of non-elongating and radially growing woody stems results from asymmetrical xylem formation. Plant Cell and Environment. 2007, 30: 646-653. 10.1111/j.1365-3040.2007.01656.x.
Schamp BS, Schurer M, Aarssen LW: Testing hypotheses for stem bending in tree saplings. International Journal of Plant Science. 2007, 168: 547-553. 10.1086/513480.
Hoson T, Saiki M, Kamisaka S, Yamashita M: Automorphogenesis and gravitropism of plant seedlings grown under microgravity conditions. Advance Space Research. 2001, 27: 933-940. 10.1016/S0273-1177(01)00157-0.
Tasaka M, Kato T, Fukaki H: The endodermis and shoot gravitropism. Trends in Plant Science. 1999, 4: 103-107. 10.1016/S1360-1385(99)01376-X.
Caspar T, Pickard B: Gravitropism in a starchless mutant of Arabidopsis. Planta. 1989, 177: 185-197. 10.1007/BF00392807.
Cosgrove D: Cellular mechanisms underlying growth asymmetry during stem gravitropism. Planta. 1997, 203 (Suppl): 130-135. 10.1007/PL00008101.
Lincoln C, Britton J, Estelle M: Growth and development of axr1 mutants of Arabidopsis. Plant Cell. 1990, 2: 1071-1080. 10.1105/tpc.2.11.1071.
Simmons C, Migliaccio F, Masson P, Caspar T, Soll D: A novel root gravitropism mutant of Arabidopsis thaliana exhibiting altered auxin physiology. Physiologia Plantarum. 1995, 93: 790-798. 10.1111/j.1399-3054.1995.tb05133.x.
Christie J, Briggs W: Blue light sensing in higher plants. Journal of Biological Chemistry. 2001, 276: 11457-11460. 10.1074/jbc.R100004200.
Ferry-Dumazet H, Houel G, Montalent P, Moreau L, Langella O, Negroni L, Vincent D, Lalanne C, de Daruvar A, Plomion C, Zivy M, Joets J: PROTICdb: A web-based application to store, track, query, and compare plant proteome data. Proteomics. 2005, 5: 2069-208127. 10.1002/pmic.200401111.
Janoudi AK, Poff K: Characterization of adaptation in phototropism of Arabidopsis thaliana. Plant Physiology. 1991, 95: 517-521. 10.1104/pp.95.2.517.
Ba EHM, Salin F, Fourcaud T, Stokes A: Reorientation strategies in leaning stems of young maritime pine (Pinus pinaster Ait) and loblolly pine (Pinus taedaL.). International Association of Wood Anatomists Journal. 2010.
Digby J, Firn RD: The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell and Environment. 1995, 18: 1434-1440. 10.1111/j.1365-3040.1995.tb00205.x.
Berthier S, Stokes A: Righting response of artificially inclined Maritime pine (Pinus pinaster Ait.) saplings to wind loading. Tree Physiology. 2006, 26: 73-79. 10.1093/treephys/26.1.73.
Plomion C, Pionneau C, Brach J, Costa P, Bailleres H: Compression wood responsive proteins in developing xylem of maritime pine Pinus pinaster Ait. Plant Physiology. 2000, 123: 959-969. 10.1104/pp.123.3.959.
Le Provost G, Paiva J, Pot D, Brach J, Plomion C: Seasonal variation in transcript accumulation in wood-forming tissues of maritime pine (Pinus pinaster Ait.) with emphasis on a cell wall glycine-rich protein. Planta. 2003, 217: 820-830. 10.1007/s00425-003-1051-2.
Gion JM, Lalanne C, Le Provost G, Ferry-Dumazet H, Paiva J, Frigerio JM, Chaumeil P, Barre A, de Daruvar A, Claverol S, Bonneu M, Sommerer N, Negroni L, Plomion C: The proteome of maritime pine wood forming tissue. Proteomics. 2005, 5: 3731-3751. 10.1002/pmic.200401197.
Kamada M, Higashitani A, Ishioka N: Proteomic analysis of Arabidopsis root gravitropism. Biological Science in Space. 2005, 19: 148-154. 10.2187/bss.19.148.
Kimbrough JM, Salinas-Mondragon R, Boss WF, Brown CS, Sederoff HW: The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiology. 2004, 136: 2790-2805. 10.1104/pp.104.044594.
Azri W, Chambon C, Herbette S, Brunel N, Coutand C, Leple JC, Rejeb I, Ammar S, Julien JL, Roeckel-Drevet P: Proteome analysis of apical and basal regions of poplar stems under gravitropic stimulation. Physiologia Plantarum. 2009, 136: 193-208. 10.1111/j.1399-3054.2009.01230.x.
Portis A: Rubisco activase - Rubisco's catalytic chaperone. Photosynthesis Research. 2003, 75: 11-27. 10.1023/A:1022458108678.
Yan S, Zhang Q, Tang Z, Su W, Sun W: Comparative proteomic analysis provides new insights into chilling stress responses in rice. Molecular & Cellular Proteomics. 2006, 5: 484-496.
Desimone M, Wagner E, Johanningmeier U: Degradation of active oxygen modified ribulose 1-5 biphosphate carboxylase oxygenase by chloroplastic proteases requires ATP hydrolysis. Planta. 1998, 205: 459-466. 10.1007/s004250050344.
Hajduch M, Rakwal R, Kumar G, Yonekura M, Pretova A: High resolution two dimensional electrophoresis sepration of proteins from metal stressed rice (Oryza sativa L.) leaves: Drastic reductions fragmentation of ribulose 1,5 biphosphate carboxylase oxygenase and induction of stress related proteins. Electrophoresis. 2001, 22: 2824-2831. 10.1002/1522-2683(200108)22:13<2824::AID-ELPS2824>3.0.CO;2-C.
Ishida H, Shimizu S, Makino A, Mae T: Light dependent fragmentation of the large subunit of ribulose 1,5-biphosphate carboxylase/oxygenase in chloroplasts isolated from wheat leaves. Planta. 1998, 204: 305-309. 10.1007/s004250050260.
Taylor N, Heazlewood J, Day D, Millar H: Differential impact of environmental stresses on the pea mitochondrial proteome. Molecular & Cellular Proteomics. 2005, 4: 1122-1133.
Limami A, Glévarec G, Ricoult C, Cliquet JB, Planchet E: Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. Journal of Experimental Botany. 2008, 59: 2325-2335. 10.1093/jxb/ern102.
Miyashita Y, Dolferus R, Ismond K, Good A: Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. The Plant Journal. 2007, 49: 1108-1121. 10.1111/j.1365-313X.2006.03023.x.
Lazova G, Stemler A: Participation of a stromal carbonic anhydrase and Rubisco in a thylacoid associated multienzyme complex isolated from soybean and poplar. Comptes Rendus de L'Academie Bulgare des Sciences. 2008, 61: 621-626.
Damerval C, De Vienne D, Zivy M, Thiellement H: Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis. 1986, 7: 52-54. 10.1002/elps.1150070108.
Ramagli L, Rodriguez L: Quantitation of microgram amounts of protein in two dimensional polyacrilamide gel electrophoresis sample buffer. Electrophoresis. 1985, 6: 559-563. 10.1002/elps.1150061109.
Shamir R, Maron-katz A, Tanay A, Linhart C, Steinfeld I, Sharan R, Shiloh Y, Elkon R: EXPANDER - an integrative program suite for microarray data analysis. BMC Bioinformatics. 2005, 6: 232-10.1186/1471-2105-6-232.
Sharan R, Shamir R: CLICK: A clustering algorithm with applications to gene expression analysis. Proceeding of the English International Conference on Intelligent System for Molecular Biology ISBM. Menlo Park, CA, USA: AAAI Press 2000, 307-316.