BACKGROUND: De-etiolation is the switch from skoto- to photomorphogenesis, enabling the heterotrophic etiolated seedling to develop into an autotrophic plant. Upon exposure to blue light (BL), reduction of hypocotyl growth rate occurs in two phases: a rapid inhibition mediated by phototropin 1 (PHOT1) within the first 30-40 min of illumination, followed by the cryptochrome 1 (CRY1)-controlled establishment of the steady-state growth rate. Although some information is available for CRY1-mediated de-etiolation, less attention has been given to the PHOT1 phase of de-etiolation. RESULTS: We generated a subtracted cDNA library using the suppression subtractive hybridization method to investigate the molecular mechanisms of BL-induced de-etiolation in tomato (Solanum lycopersicum L.), an economically important crop. We focused our interest on the first 30 min following the exposure to BL when PHOT1 is required to induce the process. Our library generated 152 expressed sequence tags that were found to be rapidly accumulated upon exposure to BL and consequently potentially regulated by PHOT1. Annotation revealed that biological functions such as modification of chromatin structure, cell wall modification, and transcription/translation comprise an important part of events contributing to the establishment of photomorphogenesis in young tomato seedlings. Our conclusions based on bioinformatics data were supported by qRT-PCR analyses the specific investigation of V-H(+)-ATPase during de-etiolation in tomato. CONCLUSIONS: Our study provides the first report dealing with understanding the PHOT1-mediated phase of de-etiolation. Using subtractive cDNA library, we were able to identify important regulatory mechanisms. The profound induction of transcription/translation, as well as modification of chromatin structure, is relevant in regard to the fact that the entry into photomorphogenesis is based on a deep reprograming of the cell. Also, we postulated that BL restrains the cell expansion by the rapid modification of the cell wall.

Department of Molecular Biology Centre of the Region Haná for Biotechnological and Agricultural Research and Faculty of Science Palacký University in Olomouc Šlechtitelů 11 CZ 783 71 Olomouc Czech Republic

Zobrazit více v PubMed

Quail PH. Photosensory perception and signalling in plant cells: new paradigms? Curr Opin Cell Biol. 2002;14:180–8. doi: 10.1016/S0955-0674(02)00309-5. PubMed DOI

Kami C, Lorrain S, Hornitschek P, Fankhauser C. Light-regulated plant growth and development. Curr Top Dev Biol. 2010;91:29–66. doi: 10.1016/S0070-2153(10)91002-8. PubMed DOI

Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J. The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development. Genes Dev. 1999;13:3259–70. doi: 10.1101/gad.13.24.3259. PubMed DOI PMC

Cosgrove DJ. Rapid suppression of growth by blue light: occurrence, time course, and general characteristics. Plant Physiol. 1981;67:584–90. doi: 10.1104/pp.67.3.584. PubMed DOI PMC

Cashmore AR, Jarillo JA, Wu Y-J, Liu D. Cryptochromes: blue light receptors for plants and animals. Science. 1999;284:760–5. doi: 10.1126/science.284.5415.760. PubMed DOI

Lin C. Plant blue-light receptors. Trends Plant Sci. 2000;5:337–42. doi: 10.1016/S1360-1385(00)01687-3. PubMed DOI

Parks BM, Cho MH, Spalding EP. Two genetically separable phases of growth inhibition induced by blue light in Arabidopsis seedlings. Plant Physiol. 1998;118:609–15. doi: 10.1104/pp.118.2.609. PubMed DOI PMC

Folta KM, Spalding EP. Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J. 2001;26:471–8. doi: 10.1046/j.1365-313x.2001.01038.x. PubMed DOI

Kinoshita T, Emi T, Tominaga M, Sakamoto K, Shigenaga A, Doi M, Shimazaki K-I. Blue-light and phosphorylation-dependent binding of a 14-3-3 protein to phototropins in stomatal guard cells of broad bean. Plant Physiol. 2003;133:1453–63. doi: 10.1104/pp.103.029629. PubMed DOI PMC

Folta KM, Leig EJ, Durham T, Spalding EP. Primary inhibition of hypocotyl growth and phototropism depend differently on phototropin-mediated increases in cytoplasmic calcium induced by blue light. Plant Physiol. 2003;133:1464–70. doi: 10.1104/pp.103.024372. PubMed DOI PMC

Shinkle JR, Jones RL. Inhibition of stem elongation in Cucumis seedlings by blue light requires calcium. Plant Physiol. 1988;86:960–6. doi: 10.1104/pp.86.3.960. PubMed DOI PMC

Klychnikov OI, Li KW, Lill H, de Boer AH. The V-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14-3-3 proteins. J Exp Bot. 2007;58:1013–23. doi: 10.1093/jxb/erl261. PubMed DOI

Bergougnoux V. The history of tomato: from domestication to biopharming. Biotechnol Adv. 2014;32:170–89. doi: 10.1016/j.biotechadv.2013.11.003. PubMed DOI

Bergougnoux V, Zalabák D, Jandová M, Novák O, Wiese-Klinkenberg A, Fellner M. Effect of blue light on endogenous isopentenyladenine and endoreduplication during photomorphogenesis and de-etiolation of tomato (Solanum lycopersicum L.) seedlings. PLoS One. 2012;7 doi: 10.1371/journal.pone.0045255. PubMed DOI PMC

Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U.S.A. 1996;93:6025–30. doi: 10.1073/pnas.93.12.6025. PubMed DOI PMC

Gulyani V, Khurana P. Identification and expression profiling of drought-regulated genes in mulberry (Morus sp.) by suppression subtractive hybridization of susceptible and tolerant cultivars. Tree Genet Genomes. 2011;7:725–38. doi: 10.1007/s11295-011-0369-3. DOI

Guo W-L, Chen R-G, Gong Z-H, Yin Y-X, Li D-W. Suppression Subtractive Hybridization Analysis of Genes Regulated by Application of Exogenous Abscisic Acid in Pepper Plant (Capsicum annuum L.) Leaves under Chilling Stress. PLoS One. 2013;8(6):e66667. doi: 10.1371/journal.pone.0066667. PubMed DOI PMC

Zhou GF, Liu YZ, Sheng O, Wei QJ, Yang CQ, Peng SA. Transcription profiles of boron-deficiency-responsive genes in citrus rootstock root by suppression subtractive hybridization and cDNA microarray. Front Plant Sci. 2015;5:795. doi: 10.3389/fpls.2014.00795. PubMed DOI PMC

Bergougnoux V, Hlaváčková V, Plotzová R, Novák O, Fellner M. The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. J Exp Bot. 2009;60:1219–30. doi: 10.1093/jxb/ern366. PubMed DOI

Miao H, Qin Y, da Silva JA T, Ye Z, Hu G. Identification of differentially expressed genes in pistils from self-incompatible Citrus reticulata by suppression subtractive hybridization. Mol Biol Rep. 2013;40:159–69. doi: 10.1007/s11033-012-2045-6. PubMed DOI

Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674–6. doi: 10.1093/bioinformatics/bti610. PubMed DOI

Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, Tohge T, Fernie AR, Stitt M, Usadel B. Mercator: a fast and simple web server genome scale functional annotation of plant sequence data. Plant Cell Environ. 2014;37:1250–8. doi: 10.1111/pce.12231. PubMed DOI

Klie S, Nikoloski Z. The choice between MapMan and gene ontology for automated gene function prediction in plant science. Front Genet. 2012;3:115. doi: 10.3389/fgene.2012.00115. PubMed DOI PMC

Dekkers BJW, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, Hilhorst HWM, Bentsink L. Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol. 2012;53:28–37. doi: 10.1093/pcp/pcr113. PubMed DOI

Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9) doi: 10.1093/nar/29.9.e45. PubMed DOI PMC

Fisher AJ, Franklin KA. Chromatin remodeling in plant light signalling. Physiol Plantarum. 2011;142:305–13. doi: 10.1111/j.1399-3054.2011.01476.x. PubMed DOI

Tessadori F, Schulkes RK, van Dreil R, Fransz P. Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J. 2007;50:848–57. doi: 10.1111/j.1365-313X.2007.03093.x. PubMed DOI

Benvenuto G, Formiggini F, Laflamme P, Malakhov M, Bowler C. The photomorphogenesis regulator DET1 binds the amino-terminal tail of histone H2B in a nucleosome context. Curr Biol. 2002;12:1529–34. doi: 10.1016/S0960-9822(02)01105-3. PubMed DOI

Carpita NC, Gibeaut DM. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993;3:1–30. doi: 10.1111/j.1365-313X.1993.tb00007.x. PubMed DOI

Van Volkenburgh E, Schmidt MG, Cleland RE. Loss of capacity for acid-induced wall loosening as the principal cause of the cessation of cell enlargement in light-grown bean leaves. Planta. 1985;163:500–5. doi: 10.1007/BF00392707. PubMed DOI

Kutschera U. Cessation of cell elongation in rye coleoptiles is accompanied by a loss of cell-wall plasticity. J Exp Bot. 1996;47:1387–94. doi: 10.1093/jxb/47.9.1387. DOI

Pauly M, Qin Q, Greene H, Albersheim P, Darvill A, York WS. Changes in the structure of xyloglucan during cell elongation. Planta. 2001;212:842–50. doi: 10.1007/s004250000448. PubMed DOI

Baumann MJ, Eklöf JM, Michel G, Kallas ÅM, Teeri TT, Czjzek M, Ill HB. Structural evidence for the evolution of xyloglucanase activity from xyloglucan endo-transglycosylases: biological implications for cell wall metabolism. Plant Cell. 2007;19:1947–63. doi: 10.1105/tpc.107.051391. PubMed DOI PMC

Miedes E, Herbers K, Sonnewald U, Lorences EP. Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits. J Agric Food Chem. 2010;58:5708–13. doi: 10.1021/jf100242z. PubMed DOI

Miedes E, Zarra I, Hoson T, Herbers K, Sonnewald U, Lorences EP. Xyloglucan endotransglucosylase and cell wall extensibility. J Plant Physiol. 2011;168:196–203. doi: 10.1016/j.jplph.2010.06.029. PubMed DOI

Nishikubo N, Takahashi J, Roos AA, Derba-Maceluch M, Piens K, Brumer H, Teeri TT, Stålbrand H, Mellerowicz EJ. Xyloglucan endo-transglycosylase-mediated xyloglucan rearrangements in developing wood of hybrid aspen. Plant Physiol. 2011;155:399–413. doi: 10.1104/pp.110.166934. PubMed DOI PMC

Zhao Q, Yuan S, Wang X, Zhang Y, Zhu H, Lu C. Restoration of mature etiolated cucumber hypocotyl cell wall susceptibility to expansion by pretreatment with fungal pectinases and EGTA in vitro. Plant Physiol. 2008;147:1874–85. doi: 10.1104/pp.108.116962. PubMed DOI PMC

Gou J-Y, Miller LM, Hou G, Yu X-H, Chen X-Y, Liu C-J. Acetylesterase-mediated deacetylation of pectin impairs cell elongation, pollen germination, and plant reproduction. Plant Cell. 2012;24:50–65. doi: 10.1105/tpc.111.092411. PubMed DOI PMC

Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997;114:295–305. doi: 10.1104/pp.114.1.295. PubMed DOI PMC

Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Bio. 2005;6:850–61. doi: 10.1038/nrm1746. PubMed DOI

Perrot-Rechenmann C. Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspect Biol. 2010;2:a001446. doi: 10.1101/cshperspect.a001446. PubMed DOI PMC

Dettmer J, Hong-Hermesdorf A, Stierhof Y-D, Schumacher K. H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell. 2006;18:715–30. doi: 10.1105/tpc.105.037978. PubMed DOI PMC

Brüx A, Liu T-Y, Krebs M, Stierhof Y-D, Lohmann JU, Miersch O, Wasternack C, Schumacher K. Reduced V-ATPase activity in the trans-Golgi network causes oxylipin-dependent hypocotyl growth inhibition in Arabidopsis. Plant Cell. 2008;20:1088–100. doi: 10.1105/tpc.108.058362. PubMed DOI PMC

Padmanaban S, Lin X, Perera I, Kawamura Y, Sze H. Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiol. 2004;134:1514–26. doi: 10.1104/pp.103.034025. PubMed DOI PMC

Bageshwar UK, Taneja-Bageshwar S, Moharram H, Binzel ML. Two isoforms of the A subunit of the vacuolar H+-ATPase in Lycopersicum esculentum: highly similar proteins but divergent patterns of tissue localization. Planta. 2005;220:632–43. doi: 10.1007/s00425-004-1377-4. PubMed DOI

Folta KM, Pontin MA, Karlin-Neumann G, Bottini R, Spalding EP. Genomic and physiological studies of early cryptochrome 1 action demonstrate roles for auxin and gibberellin in the control of hypocotyl growth by blue light. Plant J. 2003;36:203–14. doi: 10.1046/j.1365-313X.2003.01870.x. PubMed DOI