Circadian oscillatory transcriptional programs in grapevine ripening fruits

Autor: Carbonell Bejerano, Pablo; Rodriguez V.; Royo C.; Hernaiz S.; Moro-Gonzalez L.C.; Torres-Vinals M.; Martinez-Zapater J.M.; 

Tipo de documento: Artículo de revista

Revista: BMC Plant Biology. ISSN: 1471-2229. Año: 2014. Número: 1. Volumen: 14. Páginas: 1-15.

Texto completo open access 

JCR:
Edición:
Science  Área: PLANT SCIENCES  Quartil: Q1  Lugar área: 22/200  F. impacto: 3,813 

SCIMAGO:
SJR:
1,51  SNIP: 1,217 

CIRC: GRUPO A - EXCELENCIA

Referencias:

  • Dai, Z.W., Leon, C., Feil, R., Lunn, J.E., Delrot, S., Gomes, E., Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit (2013) J Exp Bot, 64, pp. 1345-1355. , 10.1093/jxb/ers396, 3598422, 23364938
  • Conde, C., Silva, P., Fontes, N., Dias, A.C.P., Tavares, R.M., Sousa, M.J., Agasse, A., Gerós, H., Biochemical changes throughout Grape Berry development and fruit and wine quality (2007) Food, 1, pp. 1-22
  • Lijavetzky, D., Carbonell-Bejerano, P., Grimplet, J., Bravo, G., Flores, P., Fenoll, J., Hellin, P., Martinez-Zapater, J.M., Berry flesh and skin ripening features in Vitis vinifera as assessed by transcriptional profiling (2012) PLoS One, 7, pp. e39547. , 10.1371/journal.pone.0039547, 3386993, 22768087
  • Teixeira, A., Eiras-Dias, J., Castellarin, S.D., Geros, H., Berry phenolics of grapevine under challenging environments (2013) Int J Mol Sci, 14, pp. 18711-18739. , 10.3390/ijms140918711, 3794804, 24030720
  • Rodriguez, A., Alquezar, B., Pena, L., Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal (2013) New Phytol, 197, pp. 36-48. , 10.1111/j.1469-8137.2012.04382.x, 23127167
  • Gil, M., Bottini, R., Berli, F., Pontin, M., Silva, M.F., Piccoli, P., Volatile organic compounds characterized from grapevine (Vitis vinifera L. cv. Malbec) berries increase at pre-harvest and in response to UV-B radiation (2013) Phytochemistry, 96, pp. 148-157
  • Davies, C., Böttcher, C., Hormonal Control of Grape Berry Ripening (2009) Grapevine Molecular Physiology &
  • Biotechnology, pp. 229-261. , Netherlands: Springer, Roubelakis-Angelakis KA
  • Kliewer, W.M., Effect of temperature on the composition of grapes grown under field and controlled conditions (1968) Proc Am Soc Horti Cult Sci, 93, pp. 797-806
  • Tarara, J.M., Lee, J., Spayd, S.E., Scagel, C.F., Berry temperature and solar radiation alter acylation, proportion, and concentration of anthocyanin in Merlot grapes (2008) Am J Enol Vitic, 59, pp. 235-247
  • Berli, F., D'Angelo, J., Cavagnaro, B., Bottini, R., Wuilloud, R., Silva, M.F., Phenolic composition in grape (Vitis vinifera L. cv. Malbec) ripened with different solar UV-B radiation levels by capillary zone electrophoresis (2008) J Agric Food Chem, 56, pp. 2892-2898. , 10.1021/jf073421+, 18412357
  • Spayd, S.E., Tarara, J.M., Mee, D.L., Ferguson, J.C., Separation of sunlight and temperature effects on the composition of Vitis vinifera cv. Merlot Berries (2002) Am J Enol Vitic, 53, pp. 171-182
  • Skinkis, P.A., Bordelon, B.P., Butz, E.M., Effects of sunlight exposure on berry and wine monoterpenes and sensory characteristics of Traminette (2010) Am J Enol Vitic, 61, pp. 147-156
  • Cortell, J.M., Kennedy, J.A., Effect of shading on accumulation of flavonoid compounds in (Vitis vinifera L.) pinot noir fruit and extraction in a model system (2006) J Agric Food Chem, 54, pp. 8510-8520. , 10.1021/jf0616560, 17061828
  • Cohen, S.D., Tarara, J.M., Kennedy, J.A., Diurnal temperature range compression Hastens Berry development and modifies flavonoid partitioning in Grapes (2011) Am J Enol Vitic, 63, pp. 112-120
  • Kliewer, W.M., Torres, R.E., Effect of Controlled Day and Night Temperatures on Grape Coloration (1972) Am J Enol Vitic, 23, pp. 71-77
  • Azuma, A., Ito, A., Moriguchi, T., Yakushiji, H., Kobayashi, S., Light emitting diode irradiation at night accelerates anthocyanin accumulation in grape skin (2012) Acta Horticult, 956, pp. 341-348
  • Carbonell-Bejerano, P., Santa Maria, E., Torres-Perez, R., Royo, C., Lijavetzky, D., Bravo, G., Aguirreolea, J., Martinez-Zapater, J.M., Thermotolerance responses in ripening berries of Vitis vinifera L. cv Muscat Hamburg (2013) Plant Cell Physiol, 54, pp. 1200-1216. , 10.1093/pcp/pct071, 23659918
  • Mori, K., Goto-Yamamoto, N., Kitayama, M., Hashizume, K., Loss of anthocyanins in red-wine grape under high temperature (2007) J Exp Bot, 58, pp. 1935-1945. , 10.1093/jxb/erm055, 17452755
  • Matus, J.T., Loyola, R., Vega, A., Pena-Neira, A., Bordeu, E., Arce-Johnson, P., Alcalde, J.A., Post-veraison sunlight exposure induces MYB-mediated transcriptional regulation of anthocyanin and flavonol synthesis in berry skins of Vitis vinifera (2009) J Exp Bot, 60, pp. 853-867. , 10.1093/jxb/ern336, 2652055, 19129169
  • Azuma, A., Yakushiji, H., Koshita, Y., Kobayashi, S., Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions (2012) Planta, 236, pp. 1067-1080. , 10.1007/s00425-012-1650-x, 22569920
  • Koyama, K., Ikeda, H., Poudel, P.R., Goto-Yamamoto, N., Light quality affects flavonoid biosynthesis in young berries of Cabernet Sauvignon grape (2012) Phytochemistry, 78, pp. 54-64
  • Harmer, S.L., The circadian system in higher plants (2009) Annu Rev Plant Biol, 60, pp. 357-377. , 10.1146/annurev.arplant.043008.092054, 19575587
  • Filichkin, S.A., Breton, G., Priest, H.D., Dharmawardhana, P., Jaiswal, P., Fox, S.E., Michael, T.P., Mockler, T.C., Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules (2011) PLoS One, 6, pp. e16907. , 10.1371/journal.pone.0016907, 3111414, 21694767
  • Huang, W., Perez-Garcia, P., Pokhilko, A., Millar, A.J., Antoshechkin, I., Riechmann, J.L., Mas, P., Mapping the core of the Arabidopsis circadian clock defines the network structure of the oscillator (2012) Science, 336, pp. 75-79. , 10.1126/science.1219075, 22403178
  • Yanovsky, M.J., Kay, S.A., Molecular basis of seasonal time measurement in Arabidopsis (2002) Nature, 419, pp. 308-312. , 10.1038/nature00996, 12239570
  • Salome, P.A., Weigel, D., McClung, C.R., The role of the Arabidopsis morning loop components CCA1, LHY, PRR7, and PRR9 in temperature compensation (2010) Plant Cell, 22, pp. 3650-3661. , 10.1105/tpc.110.079087, 3015110, 21098730
  • McWatters, H.G., Devlin, P.F., Timing in plants-a rhythmic arrangement (2011) FEBS Lett, 585, pp. 1474-1484. , 10.1016/j.febslet.2011.03.051, 21453701
  • Hotta, C.T., Gardner, M.J., Hubbard, K.E., Baek, S.J., Dalchau, N., Suhita, D., Dodd, A.N., Webb, A.A., Modulation of environmental responses of plants by circadian clocks (2007) Plant Cell Environ, 30, pp. 333-349. , 10.1111/j.1365-3040.2006.01627.x, 17263778
  • Eriksson, M.E., Webb, A.A., Plant cell responses to cold are all about timing (2011) Curr Opin Plant Biol, 14, pp. 731-737. , 10.1016/j.pbi.2011.08.005, 21937261
  • Piechulla, B., Gruissem, W., Diurnal mRNA fluctuations of nuclear and plastid genes in developing tomato fruits (1987) EMBO J, 6, pp. 3593-3599. , 553826, 3428266
  • Rodríguez-Nogales, J.M., Fernández-Fernández, E., Vila-Crespo, J., Characterisation and classification of Spanish Verdejo young white wines by volatile and sensory analysis with chemometric tools (2009) J Sci Food Agric, 89, pp. 1927-1935
  • Campo, E., Do, B.V., Ferreira, V., Valentin, D., Aroma properties of young Spanish monovarietal white wines: a study using sorting task, list of terms and frequency of citation (2008) Aust J Grape Wine Res, 14, pp. 104-115
  • Cutanda-Perez, M.C., Ageorges, A., Gomez, C., Vialet, S., Terrier, N., Romieu, C., Torregrosa, L., Ectopic expression of VlmybA1 in grapevine activates a narrow set of genes involved in anthocyanin synthesis and transport (2009) Plant Mol Biol, 69, pp. 633-648. , 10.1007/s11103-008-9446-x, 19096760
  • Walker, A.R., Lee, E., Bogs, J., McDavid, D.A., Thomas, M.R., Robinson, S.P., White grapes arose through the mutation of two similar and adjacent regulatory genes (2007) Plant J, 49, pp. 772-785. , 10.1111/j.1365-313X.2006.02997.x, 17316172
  • Kobayashi, S., Ishimaru, M., Hiraoka, K., Honda, C., Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis (2002) Planta, 215, pp. 924-933. , 10.1007/s00425-002-0830-5, 12355152
  • Boss, P.K., Thomas, M.R., Association of dwarfism and floral induction with a grape 'green revolution' mutation (2002) Nature, 416, pp. 847-850. , 10.1038/416847a, 11976683
  • Czemmel, S., Stracke, R., Weisshaar, B., Cordon, N., Harris, N.N., Walker, A.R., Robinson, S.P., Bogs, J., The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries (2009) Plant Physiol, 151, pp. 1513-1530. , 10.1104/pp.109.142059, 2773091, 19741049
  • Takata, N., Saito, S., Tanaka Saito, C., Nanjo, T., Shinohara, K., Uemura, M., Molecular phylogeny and expression of poplar circadian clock genes, LHY1 and LHY2 (2009) New Phytol, 181, pp. 808-819. , 10.1111/j.1469-8137.2008.02714.x, 19140936
  • Rawat, R., Schwartz, J., Jones, M.A., Sairanen, I., Cheng, Y., Andersson, C.R., Zhao, Y., Harmer, S.L., REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways (2009) Proc Natl Acad Sci USA, 106, pp. 16883-16888. , 10.1073/pnas.0813035106, 2757846, 19805390
  • Dal Santo, S., Tornielli, G.B., Zenoni, S., Fasoli, M., Farina, L., Anesi, A., Guzzo, F., Pezzotti, M., The plasticity of the grapevine berry transcriptome (2013) Genome Biol, 14, pp. r54. , 10.1186/gb-2013-14-6-r54, 3706941, 23759170
  • Harmer, S.L., Hogenesch, J.B., Straume, M., Chang, H.S., Han, B., Zhu, T., Wang, X., Kay, S.A., Orchestrated transcription of key pathways in Arabidopsis by the circadian clock (2000) Science, 290, pp. 2110-2113. , 10.1126/science.290.5499.2110, 11118138
  • Deluc, L.G., Grimplet, J., Wheatley, M.D., Tillett, R.L., Quilici, D.R., Osborne, C., Schooley, D.A., Cramer, G.R., Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development (2007) BMC Genomics, 8, p. 429. , 10.1186/1471-2164-8-429, 2220006, 18034876
  • Guillaumie, S., Fouquet, R., Kappel, C., Camps, C., Terrier, N., Moncomble, D., Dunlevy, J.D., Delrot, S., Transcriptional analysis of late ripening stages of grapevine berry (2011) BMC Plant Biol, 11, p. 165. , 10.1186/1471-2229-11-165, 3233516, 22098939
  • Li, Q.B., Haskell, D., Zhang, C., Sung, D.Y., Guy, C., Diurnal regulation of Hsp70s in leaf tissue (2000) Plant J, 21, pp. 373-378. , 10.1046/j.1365-313x.2000.00673.x, 10758488
  • Wang, W., Barnaby, J.Y., Tada, Y., Li, H., Tor, M., Caldelari, D., Lee, D.U., Dong, X., Timing of plant immune responses by a central circadian regulator (2011) Nature, 470, pp. 110-114. , 10.1038/nature09766, 21293378
  • Hua, J., Modulation of plant immunity by light, circadian rhythm, and temperature (2013) Curr Opin Plant Biol, 16, pp. 406-413. , 10.1016/j.pbi.2013.06.017, 23856082
  • Eulgem, T., Rushton, P.J., Schmelzer, E., Hahlbrock, K., Somssich, I.E., Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors (1999) EMBO J, 18, pp. 4689-4699. , 10.1093/emboj/18.17.4689, 1171542, 10469648
  • Marchive, C., Mzid, R., Deluc, L., Barrieu, F., Pirrello, J., Gauthier, A., Corio-Costet, M.F., Lauvergeat, V., Isolation and characterization of a Vitis vinifera transcription factor, VvWRKY1, and its effect on responses to fungal pathogens in transgenic tobacco plants (2007) J Exp Bot, 58, pp. 1999-2010. , 10.1093/jxb/erm062, 17456504
  • Holl, J., Vannozzi, A., Czemmel, S., D'Onofrio, C., Walker, A.R., Rausch, T., Lucchin, M., Bogs, J., The R2R3-MYB transcription factors MYB14 and MYB15 regulate stilbene biosynthesis in Vitis vinifera (2013) Plant Cell, 25, pp. 4135-4149. , 10.1105/tpc.113.117127, 24151295
  • Szittya, G., Silhavy, D., Molnar, A., Havelda, Z., Lovas, A., Lakatos, L., Banfalvi, Z., Burgyan, J., Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation (2003) EMBO J, 22, pp. 633-640. , 10.1093/emboj/cdg74, 140757, 12554663
  • Zhang, X., Singh, J., Li, D., Qu, F., Temperature-dependent survival of Turnip crinkle virus-infected arabidopsis plants relies on an RNA silencing-based defense that requires dcl2, AGO2, and HEN1 (2012) J Virol, 86, pp. 6847-6854. , 10.1128/JVI.00497-12, 3393596, 22496240
  • Ledger, S., Strayer, C., Ashton, F., Kay, S.A., Putterill, J., Analysis of the function of two circadian-regulated CONSTANS-LIKE genes (2001) Plant J, 26, pp. 15-22. , 10.1046/j.1365-313x.2001.01003.x, 11359606
  • Alabadi, D., Oyama, T., Yanovsky, M.J., Harmon, F.G., Mas, P., Kay, S.A., Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock (2001) Science, 293, pp. 880-883. , 10.1126/science.1061320, 11486091
  • Mizoguchi, T., Wheatley, K., Hanzawa, Y., Wright, L., Mizoguchi, M., Song, H.R., Carre, I.A., Coupland, G., LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis (2002) Dev Cell, 2, pp. 629-641. , 10.1016/S1534-5807(02)00170-3, 12015970
  • Alabadi, D., Yanovsky, M.J., Mas, P., Harmer, S.L., Kay, S.A., Critical role for CCA1 and LHY in maintaining circadian rhythmicity in Arabidopsis (2002) Curr Biol, 12, pp. 757-761. , 10.1016/S0960-9822(02)00815-1, 12007421
  • Harmer, S.L., Kay, S.A., Positive and negative factors confer phase-specific circadian regulation of transcription in Arabidopsis (2005) Plant Cell, 17, pp. 1926-1940. , 10.1105/tpc.105.033035, 1167542, 15923346
  • Gong, W., He, K., Covington, M., Dinesh-Kumar, S.P., Snyder, M., Harmer, S.L., Zhu, Y.X., Deng, X.W., The development of protein microarrays and their applications in DNA-protein and protein-protein interaction analyses of Arabidopsis transcription factors (2008) Mol Plant, 1, pp. 27-41. , 10.1093/mp/ssm009, 2756181, 19802365
  • James, A.B., Monreal, J.A., Nimmo, G.A., Kelly, C.L., Herzyk, P., Jenkins, G.I., Nimmo, H.G., The circadian clock in Arabidopsis roots is a simplified slave version of the clock in shoots (2008) Science, 322, pp. 1832-1835. , 10.1126/science.1161403, 19095940
  • Michael, T.P., Breton, G., Hazen, S.P., Priest, H., Mockler, T.C., Kay, S.A., Chory, J., A morning-specific phytohormone gene expression program underlying rhythmic plant growth (2008) PLoS Biol, 6, pp. e225. , 10.1371/journal.pbio.0060225, 2535664, 18798691
  • Bottcher, C., Burbidge, C.A., Boss, P.K., Davies, C., Interactions between ethylene and auxin are crucial to the control of grape (Vitis vinifera L.) berry ripening (2013) BMC Plant Biol, 13, p. 222. , 10.1186/1471-2229-13-222, 3878033, 24364881
  • Arana, M.V., Marin-de la Rosa, N., Maloof, J.N., Blazquez, M.A., Alabadi, D., Circadian oscillation of gibberellin signaling in Arabidopsis (2011) Proc Natl Acad Sci USA, 108, pp. 9292-9297. , 10.1073/pnas.1101050108, 3107313, 21576475
  • Kobayashi, S., Goto-Yamamoto, N., Hirochika, H., Retrotransposon-induced mutations in grape skin color (2004) Science, 304, p. 982. , 10.1126/science.1095011, 15143274
  • Lijavetzky, D., Ruiz-Garcia, L., Cabezas, J.A., De Andres, M.T., Bravo, G., Ibanez, A., Carreno, J., Martinez-Zapater, J.M., Molecular genetics of berry colour variation in table grape (2006) Mol Genet Genomics, 276, pp. 427-435. , 10.1007/s00438-006-0149-1, 16924546
  • This, P., Lacombe, T., Cadle-Davidson, M., Owens, C.L., Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1 (2007) Theor Appl Genet, 114, pp. 723-730. , 10.1007/s00122-006-0472-2, 17221259
  • Castellarin, S.D., Di Gaspero, G., Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines (2007) BMC Plant Biol, 7, p. 46. , 10.1186/1471-2229-7-46, 2147006, 17760970
  • Boss, P.K., Davies, C., Robinson, S.P., Expression of anthocyanin biosynthesis pathway genes in red and white grapes (1996) Plant Mol Biol, 32, pp. 565-569. , 10.1007/BF00019111, 8980508
  • Osterlund, M.T., Hardtke, C.S., Wei, N., Deng, X.W., Targeted destabilization of HY5 during light-regulated development of Arabidopsis (2000) Nature, 405, pp. 462-466. , 10.1038/35013076, 10839542
  • Ulm, R., Baumann, A., Oravecz, A., Mate, Z., Adam, E., Oakeley, E.J., Schafer, E., Nagy, F., Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis (2004) Proc Natl Acad Sci USA, 101, pp. 1397-1402. , 10.1073/pnas.0308044100, 337064, 14739338
  • Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Deng, X.W., Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development (2007) Plant Cell, 19, pp. 731-749. , 10.1105/tpc.106.047688, 1867377, 17337630
  • Ruffner, H.P., Hawker, J.S., Hale, C.R., Temperature and enzymic control of malate metabolism in berries of Vitis vinifera (1976) Phytochemistry, 15, pp. 1877-1880
  • Hurth, M.A., Suh, S.J., Kretzschmar, T., Geis, T., Bregante, M., Gambale, F., Martinoia, E., Neuhaus, H.E., Impaired pH homeostasis in Arabidopsis lacking the vacuolar dicarboxylate transporter and analysis of carboxylic acid transport across the tonoplast (2005) Plant Physiol, 137, pp. 901-910. , 10.1104/pp.104.058453, 1065391, 15728336
  • Stein, U., Blaich, R., Wind, R., A novel method for non-destructive determination of the sugar content and for classification of grape berries (1983) Vitis, 22, pp. 15-22
  • Fournand, D., Vicens, A., Sidhoum, L., Souquet, J.M., Moutounet, M., Cheynier, V., Accumulation and extractability of grape skin tannins and anthocyanins at different advanced physiological stages (2006) J Agric Food Chem, 54, pp. 7331-7338. , 10.1021/jf061467h, 16968102
  • Rolle, L., Segade, S.R., Torchio, F., Giacosa, S., Cagnasso, E., Marengo, F., Gerbi, V., Influence of grape density and harvest date on changes in phenolic composition, phenol extractability indices, and instrumental texture properties during ripening (2011) J Agric Food Chem, 59, pp. 8796-8805. , 10.1021/jf201318x, 21749143
  • Reid, K.E., Olsson, N., Schlosser, J., Peng, F., Lund, S.T., An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development (2006) BMC Plant Biol, 6, p. 27. , 10.1186/1471-2229-6-27, 1654153, 17105665
  • Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., Speed, T.P., Summaries of Affymetrix GeneChip probe level data (2003) Nucleic Acids Res, 31, pp. e15. , 10.1093/nar/gng015, 150247, 12582260
  • Medina, I., Carbonell, J., Pulido, L., Madeira, S.C., Goetz, S., Conesa, A., Tarraga, J., Dopazo, J., Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling (2010) Nucleic Acids Res, 38, pp. W210-W213. , 10.1093/nar/gkq388, 2896184, 20478823
  • Smyth, G.K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments (2004) Stat Appl Genet Mol Biol, 3 (1), pp. 1-25. , Article3
  • Conesa, A., Nueda, M.J., Ferrer, A., Talon, M., MaSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments (2006) Bioinformatics, 22, pp. 1096-1102. , 10.1093/bioinformatics/btl056, 16481333
  • Toronen, P., Kolehmainen, M., Wong, G., Castren, E., Analysis of gene expression data using self-organizing maps (1999) FEBS Lett, 451, pp. 142-146. , 10.1016/S0014-5793(99)00524-4, 10371154
  • Tibshirani, R., Walther, G., Hastie, T., Estimating the number of clusters in a data set via the gap statistic (2001) J R Stat Soc B, 63, pp. 411-423
  • Grimplet, J., Van Hemert, J., Carbonell-Bejerano, P., Diaz-Riquelme, J., Dickerson, J., Fennell, A., Pezzotti, M., Martinez-Zapater, J.M., Comparative analysis of grapevine whole-genome gene predictions, functional annotation, categorization and integration of the predicted gene sequences (2012) BMC Res Notes, 5, p. 213. , 10.1186/1756-0500-5-213, 3419625, 22554261
  • Al-Shahrour, F., Diaz-Uriarte, R., Dopazo, J., FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes (2004) Bioinformatics, 20, pp. 578-580. , 10.1093/bioinformatics/btg455, 14990455
  • VENNY. An interactive tool for comparing lists with Venn Diagrams http://bioinfogp.cnb.csic.es/tools/venny/index.htmlNagel, D.H., Kay, S.A., Complexity in the wiring and regulation of plant circadian networks (2012) Curr Biol, 22, pp. R648-R657. , 10.1016/j.cub.2012.07.025, 3427731, 22917516