Overexpression Of Ucp1 In Tobacco Induces Mitochondrial Biogenesis And Amplifies A Broad Stress Response

dc.creatorBarreto P.
dc.creatorOkura V.K.
dc.creatorNeshich I.A.P.
dc.creatorMaia I.D.G.
dc.creatorArruda P.
dc.date2014
dc.date2015-06-25T17:52:23Z
dc.date2015-11-26T14:16:07Z
dc.date2015-06-25T17:52:23Z
dc.date2015-11-26T14:16:07Z
dc.date.accessioned2018-03-28T21:17:04Z
dc.date.available2018-03-28T21:17:04Z
dc.identifier
dc.identifierBmc Plant Biology. Biomed Central Ltd., v. 14, n. 1, p. - , 2014.
dc.identifier14712229
dc.identifier10.1186/1471-2229-14-144
dc.identifierhttp://www.scopus.com/inward/record.url?eid=2-s2.0-84902112599&partnerID=40&md5=bc29ec27bea15827b58f5d876e89bd43
dc.identifierhttp://www.repositorio.unicamp.br/handle/REPOSIP/86265
dc.identifierhttp://repositorio.unicamp.br/jspui/handle/REPOSIP/86265
dc.identifier2-s2.0-84902112599
dc.identifier.urihttp://repositorioslatinoamericanos.uchile.cl/handle/2250/1242974
dc.descriptionBackground: Uncoupling protein one (UCP1) is a mitochondrial inner membrane protein capable of uncoupling the electrochemical gradient from adenosine-5′-triphosphate (ATP) synthesis, dissipating energy as heat. UCP1 plays a central role in nonshivering thermogenesis in the brown adipose tissue (BAT) of hibernating animals and small rodents. A UCP1 ortholog also occurs in plants, and aside from its role in uncoupling respiration from ATP synthesis, thereby wasting energy, it plays a beneficial role in the plant response to several abiotic stresses, possibly by decreasing the production of reactive oxygen species (ROS) and regulating cellular redox homeostasis. However, the molecular mechanisms by which UCP1 is associated with stress tolerance remain unknown.Results: Here, we report that the overexpression of UCP1 increases mitochondrial biogenesis, increases the uncoupled respiration of isolated mitochondria, and decreases cellular ATP concentration. We observed that the overexpression of UCP1 alters mitochondrial bioenergetics and modulates mitochondrial-nuclear communication, inducing the upregulation of hundreds of nuclear- and mitochondrial-encoded mitochondrial proteins. Electron microscopy analysis showed that these metabolic changes were associated with alterations in mitochondrial number, area and morphology. Surprisingly, UCP1 overexpression also induces the upregulation of hundreds of stress-responsive genes, including some involved in the antioxidant defense system, such as superoxide dismutase (SOD), glutathione peroxidase (GPX) and glutathione-S-transferase (GST). As a consequence of the increased UCP1 activity and increased expression of oxidative stress-responsive genes, the UCP1-overexpressing plants showed reduced ROS accumulation. These beneficial metabolic effects may be responsible for the better performance of UCP1-overexpressing lines in low pH, high salt, high osmolarity, low temperature, and oxidative stress conditions.Conclusions: Overexpression of UCP1 in the mitochondrial inner membrane induced increased uncoupling respiration, decreased ROS accumulation under abiotic stresses, and diminished cellular ATP content. These events may have triggered the expression of mitochondrial and stress-responsive genes in a coordinated manner. Because these metabolic alterations did not impair plant growth and development, UCP1 overexpression can potentially be used to create crops better adapted to abiotic stress conditions. © 2014 Barreto et al.; licensee BioMed Central Ltd.
dc.description14
dc.description1
dc.description
dc.description
dc.descriptionNedergaard, J., Ricquier, D., Kozak, L.P., Uncoupling proteins: current status and therapeutic prospects (2005) EMBO Rep, 6, pp. 917-921. , 10.1038/sj.embor.7400532, 1369193, 16179945
dc.descriptionKrauss, S., Zhang, C.Y., Lowell, B.B., The mitochondrial uncoupling-protein homologues (2005) Nat Rev Mol Cell Biol, 6, pp. 248-261. , 10.1038/nrm1592, 15738989
dc.descriptionAndrews, Z.B., Diano, S., Horvath, T.L., Mitochondrial uncoupling proteins in the CNS: in support of function and survival (2005) Nat Rev Neurosci, 6, pp. 829-840. , 10.1038/nrn1767, 16224498
dc.descriptionKajimura, S., Seale, P., Spiegelman, B.M., Transcriptional control of brown fat development (2010) Cell Metab, 11, pp. 257-262. , 10.1016/j.cmet.2010.03.005, 2857670, 20374957
dc.descriptionVercesi, A.E., Martins, L.S., Silva, M.A.P., Leite, H.M.F., Cuccovia, I.M., Chaimovich, H., PUMPing plants (1995) Nature, 375, p. 24
dc.descriptionMaia, I.G., Benedetti, C.E., Leite, A., Turcinelli, S.R., Vercesi, A.E., Arruda, P., AtPUMP: an Arabidopsis gene encoding a plant uncoupling mitochondrial protein (1998) FEBS Lett, 429, pp. 403-406. , 10.1016/S0014-5793(98)00634-6, 9662458
dc.descriptionBorecky, J., Nogueira, F.T.S., Oliveira, K.A.P., Maia, I.G., Vercesi, A.E., Arruda, P., The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots (2006) J Exp Bot, 57, pp. 849-864. , 10.1093/jxb/erj070, 16473895
dc.descriptionVercesi, A.E., Borecký, J., Maia, I.G., Arruda, P., Cuccovia, I.M., Chaimovich, H., Plant uncoupling mitochondrial proteins (2006) Annu Rev Plant Biol, 57, pp. 383-404. , 10.1146/annurev.arplant.57.032905.105335, 16669767
dc.descriptionIto-Inaba, Y., Hida, Y., Mora, H., Inaba, T., Molecular identity of uncoupling proteins in thermogenic skunk cabbage (2008) Plant Cell Physiol, 49, pp. 1911-1916. , 10.1093/pcp/pcn161, 18974196
dc.descriptionJezek, P., Borecký, J., Zácková, M., Costa, A.D., Arruda, P., Possible basic and specific functions of plant mitochondrial uncoupling protein (pUCP) (2001) Biosci Rep, 21, pp. 237-245. , 10.1023/A:1013660611154, 11725872
dc.descriptionBrandalise, M., Maia, I.G., Borecký, J., Vercesi, A.E., Arruda, P., Overexpression of plant mitochondrial uncoupling protein in transgenic tobacco increases tolerance to oxidative stress (2003) J Bioenerg Biomembr, 35, pp. 205-209
dc.descriptionBegcy, K., Mariano, E.D., Mattiello, L., Nunes, A.V., Mazzafera, P., Maia, I.G., Menossi, M., An Arabidopsis mitochondrial uncoupling protein confers tolerance to draught and salt stress in transgenic tobacco plants (2011) Plos One, 6, pp. e23776. , 10.1371/journal.pone.0023776, 3166057, 21912606
dc.descriptionChen, S., Liu, A., Zhang, S., Li, C., Chang, R., Liu, D., Ahammed, G.J., Lin, X., Overexpression of mitochondrial uncoupling protein conferred resistance to heat stress an Botrytis cinerea infection in tomato (2013) Plant Physiol Biochem, 73, pp. 245-253
dc.descriptionSweetlove, L.J., Lytovchenko, A., Morgan, M., Nunes-Nesi, A., Taylor, N.L., Baxter, C.J., Eickmeier, A., Fernie, A.R., Mitochondrial uncoupling protein is required for efficient photosynthesis (2006) Proc Natl Acad Sci U S A, 103, pp. 19587-19592. , 10.1073/pnas.0607751103, 1748269, 17148605
dc.descriptionRhoads, D.M., Umbach, A.L., Subbaiah, C.C., Siedow, J.N., Mitochondrial reactive oxygen species: contribution to oxidative stress and interorganellar signaling (2006) Plant Physiol, 141, pp. 357-366. , 10.1104/pp.106.079129, 1475474, 16760488
dc.descriptionRhoads, D.M., Subbaiah, C.C., Mitochondrial retrograde regulation in plants (2007) Mitochondrion, 7, pp. 177-194. , 10.1016/j.mito.2007.01.002, 17320492
dc.descriptionWoodson, J.D., Chory, J., Coordination of gene expression between organellar and nuclear genomes (2008) Nat Rev Genet, 9, pp. 383-395. , 10.1038/nrg2348, 18368053
dc.descriptionRyan, M.T., Hoogenrad, M.J., Mitochondrial-nuclear communications (2007) Annu Rev Biochem, 76, pp. 701-722. , 10.1146/annurev.biochem.76.052305.091720, 17227225
dc.descriptionPesaresi, P., Schneider, A., Kleine, T., Leister, D., Interorganellar communication (2007) Curr Opin Plant Biol, 10, pp. 600-606. , 10.1016/j.pbi.2007.07.007, 17719262
dc.descriptionJung, H.S., Chory, J., Signaling between chloroplasts and the nucleus: can a systems biology approach bring clarity to a complex and highly regulated pathway (2009) Plant Physiol, 152, pp. 453-459. , 2815895, 19933385
dc.descriptionWelchen, E., Garcia, L., Mansilla, N., Gonzalez, D.H., Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements (2013) Front Plant Sci, 4, p. 551
dc.descriptionZabaleta, E., Heiser, V., Grohmann, L., Brennicke, A., Promoters of nuclear-encoded respiratory chain complex I genes from Arabidopsis thaliana contain a region essential for anther/pollen-specific expression (1998) Plant J, 156, pp. 49-59
dc.descriptionBinder, S., Brennicke, A., Gene expression in plant mitochondria: transcriptional and post-transcriptional control (2003) Philos Trans R Soc Lond B Biol Sci, 3586, pp. 181-188
dc.descriptionGiegè, P., Sweetlove, L.J., Congat, V., Leaver, C.J., Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis (2005) Plant Cell, 17, pp. 1497-1512. , 10.1105/tpc.104.030254, 1091770, 15829605
dc.descriptionHammani, K., Gobert, A., Hleibieh, K., Choulier, L., Small, L., Giegè, P., An Arabidopsis dual-localized pentatricopeptide repeat protein interacts with nuclear proteins involved in gene expression regulation (2011) Plant Cell, 23, pp. 730-740. , 10.1105/tpc.110.081638, 3077779, 21297037
dc.descriptionRoschzttardtz, H., Fuentes, I., Vásquez, M., Corvalán, C., León, G., Gómez, I., Araya, A., Jordana, X., A nuclear gene encoding the iron-sulfur subunit of mitochondrial complex II is regulated by B3 domain transcription factors during seed development in Arabidopsis thaliana (2009) Plant Physiol, 150, pp. 84-95. , 10.1104/pp.109.136531, 2675723, 19261733
dc.descriptionVan Aken, O., Zhang, B., Law, S., Narsai, R., Whelan, J., AtWKRY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins (2013) Plant Physiol, 162, pp. 254-271. , 10.1104/pp.113.215996, 3641207, 23509177
dc.descriptionGiraud, E., Ng, S., Carrie, C., Duncan, O., Low, J., Lee, C.P., Van Aken, O., Whelan, J., TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana (2010) Plant Cell, 22, pp. 3921-3934. , 10.1105/tpc.110.074518, 3027163, 21183706
dc.descriptionDe Clercq, I., Vermeirssen, V., Van Aken, O., Vandepoele, K., Murcha, M.W., Law, S.R., Inzé, A., Van Breusegem, F., The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis (2013) Plant Cell, 25, pp. 3472-3490. , 10.1105/tpc.113.117168, 24045019
dc.descriptionÖlçer, H., Lloyd, J.C., Raines, C.A., Photosynthetic capacity is differentially affected by reductions in sedoheptulose-1,7-biphosphatase activity during leaf development in transgenic tobacco plants (2001) Plant Physiol, 125, pp. 982-989. , 10.1104/pp.125.2.982, 64898, 11161054
dc.descriptionRogalski, M., Schöttler, M.A., Thiele, W., Schulze, W.X., Bock, R., Rpl33, a nonessential plastid-encoded ribosomal protein in tobacco, is required under cold stress conditions (2008) Plant Cell, 20, pp. 2221-2237. , 10.1105/tpc.108.060392, 2553612, 18757552
dc.descriptionUnseld, M., Marienfeld, J.R., Brandt, P., Brennicke, A., The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotide (1997) Nat Genet, 15, pp. 57-61. , 10.1038/ng0197-57, 8988169
dc.descriptionDickinson, A., Yeung, K.Y., Donoghue, J., Baker, M.J., Kelly, R.D.W., McKenzie, M., Jhons, T.J., St John, J.C., The regulation of mitochondrial DNA copy number in glioblastoma cells (2013) Cell Death Differ, 20, pp. 1644-1653. , 10.1038/cdd.2013.115, 3824586, 23995230
dc.descriptionKlodmann, J., Senkler, M., Rode, C., Braun, H.P., Defining the protein complex proteome of plant mitochondria (2011) Plant Physiol, 157, pp. 587-598. , 10.1104/pp.111.182352, 3192552, 21841088
dc.descriptionPadimam, M., Reddy, V.S., Beachy, R.N., Fauquet, C.M., Molecular characterization of a plant mitochondrial chaperone GrpE (1999) Plant Mol Biol, 39, pp. 871-881. , 10.1023/A:1006143305907, 10344193
dc.descriptionFiorani, F., Umbach, A.L., Siedow, J.N., The alternative oxidase of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants (2005) Plant Physiol, 139, pp. 1795-1805. , 10.1104/pp.105.070789, 1310560, 16299170
dc.descriptionSmolková, K., Jezek, P., The role of mitochondrial NADPH-dependent isocitrate dehydrogenase in cancer cells (2012) Int J Cell Biol, 212, pp. 1-12
dc.descriptionRobert, N., D'Erfurth, I., Marmagne, A., Erhardt, M., Allot, M., Boivin, K., Gissot, L., Filleur, S., Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria (2012) Plant Mol Biol, 78, pp. 431-446. , 10.1007/s11103-012-9874-5, 22294207
dc.descriptionLeadsham, J.E., Sanders, G., Giannaki, S., Bastow, E.L., Hutton, R., Naeimi, W.R., Breitenbach, M., Gourlay, C.W., Loss of cytochrome c oxidase promotes RAS-dependent ROS production from the ER resident NADPH oxidase, Yno1p, in yeast (2013) Cell Metab, 18, pp. 279-286. , 10.1016/j.cmet.2013.07.005, 23931758
dc.descriptionSmith, A.M.O., Ratcliffe, G., Sweetlove, L.J., Activation and function of mitochondrial uncoupling protein in plants (2004) J Biol Chem, 279, pp. 51944-51952. , 10.1074/jbc.M408920200, 15456782
dc.descriptionLiesa, M., Shirihai, O.S., Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure (2013) Cell Metab, 17, pp. 491-506. , 10.1016/j.cmet.2013.03.002, 23562075
dc.descriptionSchneider, C.A., Rasband, W.S., Eliceir, K.W., NIH image to ImageJ: 25 years of image analysis (2012) Nat Methods, 9, pp. 671-675. , 10.1038/nmeth.2089, 22930834
dc.descriptionLiu, X., Hajnóczky, G., Altered fusion dynamics underlie unique morphological changes in mitochondria during hypoxia-reoxygenation stress (2011) Cell Death Differ, 18, pp. 1561-1572. , 10.1038/cdd.2011.13, 3172112,3172112, 21372848
dc.descriptionUpdate on activities at the universal protein resource (UniProt) in 2013 (2013) Nucleic Acids Res, 41, pp. D43-D47. , 3531094, 23161681, The UniProt Consortium
dc.descriptionTatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Natale, D.A., The COG database: an updated version includes eukaryotes (2003) BMC Bioinforma, 4, p. 41
dc.descriptionLamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Huala, E., The Arabidopsis information resource (TAIR): improved gene annotation and new tools (2012) Nucleic Acids Res, 40, pp. 1202-1210
dc.descriptionEmanuelsson, O., Brunak, S., Heijne, V.J., Nielsen, H., Locating proteins in the cell using TargetP, SignalP, and related tools (2007) Nat Protoc, 2, pp. 953-971. , 10.1038/nprot.2007.131, 17446895
dc.descriptionOelkrug, R., Kutschke, M., Meyer, C.W., Heldmaier, G., Jastroch, M., Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria (2010) J Biol Chem, 285, pp. 21961-21968. , 10.1074/jbc.M110.122861, 2903373, 20466728
dc.descriptionVafai, S.B., Mootha, V.K., Mitochondrial disorders as windows into an ancient organelle (2012) Nature, 491, pp. 374-383. , 10.1038/nature11707, 23151580
dc.descriptionWu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Spiegelman, B.M., Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1 (1999) Cell, 98, pp. 115-124. , 10.1016/S0092-8674(00)80611-X, 10412986
dc.descriptionMiyoshi, N., Oubrahim, H., Chock, P.B., Stadtman, E.R., Age-dependent cell death and the role of ATP in hydrogen-peroxide-induced apoptosis and necrosis (2006) Proc Natl Acad Sci U S A, 103, pp. 1727-1731. , 10.1073/pnas.0510346103, 1413652, 16443681
dc.descriptionMoghadam, A.A., Ebrahimie, E., Taghavi, S.M., Niazi, A., Babgohari, M.Z., Deihimi, T., Djavaheri, M., Ramezani, A., How the nucleus and mitochondria communicate in energy production during stress: nuclear MtATP6, an early-stress responsive gene, regulates the mitochondrial F1F0;-ATP synthase complex (2013) Mol Biotechnol, 54, pp. 756-769. , 10.1007/s12033-012-9624-6, 23208548
dc.descriptionLin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Spiegelman, B.M., Transcriptional co-activator PGC-1 alpha drives the formation of slow twitch muscle fibres (2002) Nature, 418, pp. 797-801. , 10.1038/nature00904, 12181572
dc.descriptionPeters, K., Niessen, M., Peterhansel, C., Spath, B., Holzle, A., Binder, S., Marchfelder, A., Braun, H.P., Complex I-complex II ratio strongly differs in various organs of Arabidopsis thaliana (2012) Plant Mol Biol, 79, pp. 273-284. , 10.1007/s11103-012-9911-4, 22527752
dc.descriptionLaw, S.R., Narsai, R., Taylor, N.L., Dellanoy, E., Carrie, C., Giraud, E., Millar, A.H., Whelan, J., Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination (2012) Plant Physiol, 158, pp. 1610-1627. , 10.1104/pp.111.192351, 3320173, 22345507
dc.descriptionBerg, J.M., Tymoczko, J.L., Stryer, L., Biochemistry (2002) The Citric Acid Cycle, , New York: W H Freeman, 5
dc.descriptionPfanner, N., Geissler, A., Versatility of the mitochondrial protein import machinery (2001) Nat Rev Mol Cell Biol, 2, pp. 339-349. , 10.1038/35073006, 11331908
dc.descriptionSchleiffe, E., Becker, T., Common ground for protein translocation: access control for mitochondria and chloroplasts (2011) Nat Rev Mol Cell Biol, 12, pp. 48-59. , 10.1038/nrm3027, 21139638
dc.descriptionSearcy, D.G., Metabolic integration during the evolutionary origin of mitochondria (2003) Cell Res, 13, pp. 229-238. , 10.1038/sj.cr.7290168, 12974613
dc.descriptionKleine, T., Leister, D., Retrograde signals galore (2013) Front Plant Sci, 4, pp. 1-3. , 3551192, 23346092
dc.descriptionStael, S., Wurzinger, B., Mair, A., Mehlmer, N., Vothknecht, U.C., Teige, M., Plant organellar calcium signaling: an emerging field (2012) J Exp Bot, 63, pp. 1525-1542. , 10.1093/jxb/err394, 3966264, 22200666
dc.descriptionClapham, D.E., Calcium signaling (2007) Cell, 131, pp. 1047-1058. , 10.1016/j.cell.2007.11.028, 18083096
dc.descriptionTarasov, A.I., Griffiths, E.J., Rutter, G.A., Regulation of ATP production by mitochondrial Ca + 2 (2012) Cell Calcium, 52, pp. 28-35. , 10.1016/j.ceca.2012.03.003, 3396849, 22502861
dc.descriptionAlam, M.R., Groschner, L.N., Parichatikanond, W., Kuo, L., Bondarenko, A.I., Rost, R., Waldeck-Weiermaier, M., Graier, W.F., Mitochondrial Ca2+ uptake 1 (MICU1) and mitochondrial Ca + 2 uniporter (MCU) contribute to metabolism secretion coupling in clonal pancreatic β-cells (2012) J Biol Chem, 287, pp. 34445-34454. , 10.1074/jbc.M112.392084, 3464549,3464549, 22904319
dc.descriptionPalty, R., Silverman, W.F., Herschfinkel, M., Caporale, T., Sensi, S.L., Parnis, J., Nolte, C., Sekler, I., NCLX is an essential component of mitochondrial Na+/Ca+2 exchange (2010) Proc Natl Acad Sci U S A, 107, pp. 436-441. , 10.1073/pnas.0908099107, 2806722, 20018762
dc.descriptionMailloux, R.J., Harper, M.E., Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins (2012) Trends Endocrinol Metab, 23, pp. 451-458. , 10.1016/j.tem.2012.04.004, 22591987
dc.descriptionSi, Y., Palani, S., Jayaraman, A., Lee, K., Effects of forced uncoupling protein1 expression in 3T3-L1 cells on mitochondrial function and lipid metabolism (2007) J Lipid Res, 48, pp. 826-836. , 10.1194/jlr.M600343-JLR200, 17202129
dc.descriptionWang, D.Y., Zhang, Q., Liu, Y., Lin, Z.F., Zhang, S.X., Sun, M.X., The levels of male gametic mitochondrial DNA are highly regulated in angiosperms with regard to mitochondrial inheritance (2010) Plant Cell, 22, pp. 2402-2416. , 10.1105/tpc.109.071902, 2929101, 20605854, Sodmergen
dc.descriptionYoo, S.D., Cho, Y.H., Sheen, J., Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis (2007) Nat Protoc, 2, pp. 1565-1572. , 10.1038/nprot.2007.199, 17585298
dc.descriptionOgawa, K., Hatano-Iwasaki, A., Yanagida, M., Iwabuchi, M., Level of glutathione is regulated by ATP-dependent ligation of glutamate and cysteine through photosynthesis in Arabidopsis thaliana: mechanism of strong interaction of light intensity with flowering (2004) Plant Cell Physiol, 45, pp. 1-8. , 10.1093/pcp/pch008, 14749480
dc.descriptionKeech, O., Dizengremel, P., Gardestrom, P., Preparation of leaf mitochondria from Arabidopsis thaliana (2005) Physiol Plant, 124, pp. 403-409
dc.descriptionGrabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Regev, A., Full-length transcriptome assembly from RNA-seq data without reference genome (2011) Nat Biotechnol, 29, pp. 644-652. , 10.1038/nbt.1883, 3571712, 21572440
dc.descriptionWagner, G.P., Kin, K., Lynch, V.J., Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples (2012) Theory Biosci, 131, pp. 281-285. , 10.1007/s12064-012-0162-3, 22872506
dc.descriptionLangmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome (2009) Genome Biol, 10, pp. R25. , 10.1186/gb-2009-10-3-r25, 2690996, 19261174
dc.descriptionThe tomato genome sequence provides insights into fleshy fruit evolution (2012) Nature, 485, pp. 635-641. , 10.1038/nature11119, 3378239, 22660326, Tomato Genome Consortium
dc.descriptionNaika, M., Shameer, K., Mathew, O.K., Gowda, R., Sowdhamini, R., STIFDB2: An updated version of plant stress-responsive transcription factor database with additional stress signals, stress-responsive transcription factor binding sites and stress-responsive genes in Arabidopsis and rice (2013) Plant Cell Physiol, 54, pp. 1-15. , 10.1093/pcp/pcs172, 23300091
dc.languageen
dc.publisherBioMed Central Ltd.
dc.relationBMC Plant Biology
dc.rightsaberto
dc.sourceScopus
dc.titleOverexpression Of Ucp1 In Tobacco Induces Mitochondrial Biogenesis And Amplifies A Broad Stress Response
dc.typeArtículos de revistas


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