Artículo

Moschen, S.; Bengoa Luoni, S.; Di Rienzo, J.A.; Caro, M.del.P.; Tohge, T.; Watanabe, M.; Hollmann, J.; González, S.; Rivarola, M.; García-García, F.; Dopazo, J.; Hopp, H.E.; Hoefgen, R.; Fernie, A.R.; Paniego, N.; Fernández, P.; Heinz, R.A. "Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower" (2016) Plant Biotechnology Journal. 14(2):719-734
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Leaf senescence is a complex process, which has dramatic consequences on crop yield. In sunflower, gap between potential and actual yields reveals the economic impact of senescence. Indeed, sunflower plants are incapable of maintaining their green leaf area over sustained periods. This study characterizes the leaf senescence process in sunflower through a systems biology approach integrating transcriptomic and metabolomic analyses: plants being grown under both glasshouse and field conditions. Our results revealed a correspondence between profile changes detected at the molecular, biochemical and physiological level throughout the progression of leaf senescence measured at different plant developmental stages. Early metabolic changes were detected prior to anthesis and before the onset of the first senescence symptoms, with more pronounced changes observed when physiological and molecular variables were assessed under field conditions. During leaf development, photosynthetic activity and cell growth processes decreased, whereas sucrose, fatty acid, nucleotide and amino acid metabolisms increased. Pathways related to nutrient recycling processes were also up-regulated. Members of the NAC, AP2-EREBP, HB, bZIP and MYB transcription factor families showed high expression levels, and their expression level was highly correlated, suggesting their involvement in sunflower senescence. The results of this study thus contribute to the elucidation of the molecular mechanisms involved in the onset and progression of leaf senescence in sunflower leaves as well as to the identification of candidate genes involved in this process. © 2016 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd.

Registro:

Documento: Artículo
Título:Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower
Autor:Moschen, S.; Bengoa Luoni, S.; Di Rienzo, J.A.; Caro, M.del.P.; Tohge, T.; Watanabe, M.; Hollmann, J.; González, S.; Rivarola, M.; García-García, F.; Dopazo, J.; Hopp, H.E.; Hoefgen, R.; Fernie, A.R.; Paniego, N.; Fernández, P.; Heinz, R.A.
Filiación:Instituto de Biotecnología, Centro de Investigaciones en Ciencias Agronómicas y Veterinarias, Instituto Nacional de Tecnología Agropecuaria, Hurlingham, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Ciudad Autónoma de Buenos Aires, Argentina
Escuela de Ciencia y Tecnología, Universidad Nacional de San Martín, San Martín, Argentina
Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, Córdoba, Argentina
Instituto Superior de Investigaciones Biológicas, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional de Tucumán, San Miguel de Tucumán, Argentina
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam-Golm, Germany
Institute of Botany, Christian-Albrechts-University of Kiel, Kiel, Germany
Department of Bioinformatics and Genomics, Centro de Investigación Príncipe Felipe, Valencia, Spain
Functional Genomics Node, National Institute of Bioinformatics, Centro de Investigación Príncipe Felipe, Valencia, Spain
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina
Palabras clave:Candidate genes; Data integration; Leaf senescence; Metabolomics; Sunflower; Transcriptomics; ion; messenger RNA; transcription factor; DNA microarray; gene expression profiling; gene expression regulation; gene ontology; genetics; growth, development and aging; mass fragmentography; metabolism; metabolomics; plant gene; plant leaf; principal component analysis; procedures; sunflower; Gas Chromatography-Mass Spectrometry; Gene Expression Profiling; Gene Expression Regulation, Plant; Gene Ontology; Genes, Plant; Helianthus; Ions; Metabolomics; Oligonucleotide Array Sequence Analysis; Plant Leaves; Principal Component Analysis; RNA, Messenger; Transcription Factors
Año:2016
Volumen:14
Número:2
Página de inicio:719
Página de fin:734
DOI: http://dx.doi.org/10.1111/pbi.12422
Título revista:Plant Biotechnology Journal
Título revista abreviado:Plant Biotechnol. J.
ISSN:14677644
CAS:Ions; RNA, Messenger; Transcription Factors
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_14677644_v14_n2_p719_Moschen

Referencias:

  • Abbasi, A.-R., Saur, A., Hennig, P., Tschiersch, H., Hajirezaei, M., Hofius, D., Sonnewald, U., Voll, L.M., Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence (2009) Plant Cell Environ., 32, pp. 144-157
  • Aguirrezábal, L.A.N., Lavaud, Y., Dosio, G.A.A., Izquierdo, N.G., Andrade, F.H., González, L.M., Weight per seed and oil concentration in a sunflower hybrid are accounted for by intercepted solar radiation during a definite period of seed filling (2003) Crop Sci., 43, pp. 152-161
  • Almeida, J., Quadrana, L., Asís, R., Setta, N., de Godoy, F., Bermúdez, L., Otaiza, S.N., Rossi, M., Genetic dissection of vitamin E biosynthesis in tomato (2011) J. Exp. Bot., 62, pp. 3781-3798
  • Al-Shahrour, F., Minguez, P., Vaquerizas, J.M., Conde, L., Dopazo, J., BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments (2005) Nucleic Acids Res., 33, pp. W460-W464
  • Al-Shahrour, F., Arbiza, L., Dopazo, H., Huerta-Cepas, J., Minguez, P., Montaner, D., Dopazo, J., From genes to functional classes in the study of biological systems (2007) BMC Bioinformatics, 8, p. 114
  • Araújo, W.L., Ishizaki, K., Nunes-Nesi, A., Larson, T.R., Tohge, T., Krahnert, I., Witt, S., Fernie, A.R., Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria (2010) Plant Cell, 22, pp. 1549-1563
  • Araújo, W.L., Tohge, T., Ishizaki, K., Leaver, C.J., Fernie, A.R., Protein degradation - an alternative respiratory substrate for stressed plants (2011) Trends Plant Sci., 16, pp. 489-498
  • Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Sherlock, G., Gene ontology: tool for the unification of biology. The Gene Ontology Consortium (2000) Nat. Genet., 25, pp. 25-29
  • Balazadeh, S., Riaño-Pachón, D.M., Mueller-Roeber, B., Transcription factors regulating leaf senescence in Arabidopsis thaliana (2008) Plant Biol., 10, pp. 63-75
  • Balazadeh, S., Wu, A., Mueller-Roeber, B., Salt-triggered expression of the ANAC092-dependent senescence regulon in Arabidopsis thaliana (2010) Plant Signal. Behav., 5, p. 733
  • Balazadeh, S., Kwasniewski, M., Caldana, C., Mehrnia, M., Zanor, M.I., Xue, G.-P., Mueller-Roeber, B., ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana (2011) Mol Plant, 4, pp. 346-360
  • Balazadeh, S., Garapati, P., Xue, G., Mueller-Roeber, B., A transcription factor upstream of ORE1 and GLK1 integrates ABA signalling with drought-induced senescence (2013) 6th European Workshop on Leaf Senescence, , 14-18 October. INRA, Versailles, France
  • Balazadeh, S., Schildhauer, J., Araújo, W.L., Munné-Bosch, S., Fernie, A.R., Proost, S., Humbeck, K., Mueller-Roeber, B., Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences (2014) J. Exp. Bot., pp. 1-18
  • Balibrea Lara, M.E., Gonzalez Garcia, M.-C., Fatima, T., Ehness, R., Lee, T.K., Proels, R., Tanner, W., Roitsch, T., Extracellular invertase is an essential component of cytokinin-mediated delay of senescence (2004) Plant Cell, 16, pp. 1276-1287
  • Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing (1995) J. R. Stat. Soc. Series B Methodol., 57, pp. 289-300
  • Bernard, S., Habash, D., The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling (2009) New Phytol., 182, pp. 608-620
  • Besseau, S., Li, J., Palva, E.T., WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana (2012) J. Exp. Bot., 63, pp. 2667-2679
  • Blom-Zandstra, G., Lampe, J.E.M., The effect of chloride and sulphate salts on the nitrate content in lettuce plants (Lactuca sativa L.) (1983) J. Plant Nutr., 6, pp. 611-628
  • Breeze, E., Harrison, E., Page, T., Warner, N., Shen, C., Zhang, C., Buchanan-Wollaston, V., Transcriptional regulation of plant senescence: from functional genomics to systems biology (2008) Plant Biol (Stuttg), 10, pp. 99-109
  • Breeze, E., Harrisona, E., McHattiea, S., Hughesa, L., Hickmana, R., Hilla, C., Kiddle, S., Buchanan-wollaston, V., High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation (2011) Plant Cell, 23, pp. 873-894
  • Brugière, N., Dubois, F., Masclaux, C., Sangwan, R.S., Hirel, B., Immunolocalization of glutamine synthetase in senescing tobacco (Nicotiana tabacum L.) leaves suggests that ammonia assimilation is progressively shifted to the mesophyll cytosol (2000) Planta, 211, pp. 519-527
  • Bu, Q., Jiang, H., Li, C.-B., Zhai, Q., Zhang, J., Wu, X., Sun, J., Li, C., Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses (2008) Cell Res., 18, pp. 756-767
  • Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T., Pink, D., The molecular analysis of leaf senescence-a genomics approach (2003) Plant Biotechnol. J., 1, pp. 3-22
  • Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P.O., Nam, H.G., Lin, J.-F., Leaver, C.J., Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis (2005) Plant J., 42, pp. 567-585
  • Cabello, P., Agüera, E., la Haba, P., Metabolic changes during natural ageing in sunflower (Helianthus annuus) leaves: expression and activity of glutamine synthetase isoforms are regulated differently during senescence (2006) Physiol. Plant., 128, pp. 175-185
  • Carrión, C.A., Costa, M.L., Martínez, D.E., Mohr, C., Humbeck, K., Guiamet, J.J., In vivo inhibition of cysteine proteases provides evidence for the involvement of "senescence-associated vacuoles" in chloroplast protein degradation during dark-induced senescence of tobacco leaves (2013) J. Exp. Bot., 64, pp. 4967-4980
  • Charlton, W.L., Johnson, B., Graham, I.A., Baker, A., Non-coordinate expression of peroxisome biogenesis, beta-oxidation and glyoxylate cycle genes in mature Arabidopsis plants (2005) Plant Cell Rep., 23, pp. 647-653
  • Chen, G.-H., Chan, Y.-L., Liu, C.-P., Wang, L.-C., Ethylene response pathway is essential for ARABIDOPSIS A-FIFTEEN function in floral induction and leaf senescence (2012) Plant Signal. Behav., 7, pp. 457-460
  • Chen, G.-H., Liu, C.-P., Chen, S.-C., Wang, L.-C., Role of ARABIDOPSIS A-FIFTEEN in regulating leaf senescence involves response to reactive oxygen species and is dependent on ETHYLENE INSENSITIVE2 (2012) J. Exp. Bot., 63, pp. 275-292
  • Collakova, E., DellaPenna, D., The role of homogentisate phytyltransferase and other tocopherol pathway enzymes in the regulation of tocopherol synthesis during abiotic stress (2003) Plant Physiol., 133, pp. 930-940
  • Davies, P.J., Gan, S., Towards an integrated view of monocarpic plant senescence (2012) Russ. J. Plant Physiol., 59, pp. 467-478
  • DelaVega, A.J., Cantore, M.A., Sposaro, M.M., Trápani, N., López Pereira, M., Hall, A.J., Canopy stay-green and yield in non-stressed sunflower (2011) Field. Crop. Res., 121, pp. 175-185
  • Desclos, M., Etienne, P., Coquet, L., Jouenne, T., Bonnefoy, J., Segura, R., Reze, S., Avice, J.-C., A combined 15N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation (2009) Proteomics, 9, pp. 3580-3608
  • Dezar, C.A., Fedrigo, G.V., Chan, R.L., The promoter of the sunflower HD-Zip protein gene Hahb4 directs tissue-specific expression and is inducible by water stress, high salt concentrations and ABA (2005) Plant Sci., 169, pp. 447-456
  • Dezar, C.A., Gago, G.M., Gonzalez, D.H., Chan, R.L., Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants (2005) Transgenic Res., 14, pp. 429-440
  • Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M., Robledo, C.W., InfoStat versión 2014 (2013), http://www.infostat.com.ar, Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. URL() InfoStat; Diaz, C., Purdy, S., Christ, A., Morot-Gaudry, J.-F., Wingler, A., Masclaux-Daubresse, C., Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach (2005) Plant Physiol., 1, pp. 898-908
  • Dietz, K.-J., Vogel, M.O., Viehhauser, A., AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling (2010) Protoplasma, 245, pp. 3-14
  • van Doorn, W.G., Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? (2008) J. Exp. Bot., 59, pp. 1963-1972
  • Dosio, G.A.A., Aguirreza, L.A.N., Andrade, F.H., Pereyra, V.R., Aguirrezábal, L.A.N., Solar radiation intercepted during seed filling and oil production in two sunflower hybrids (2000) Crop Sci., 1644, pp. 1637-1644
  • Dubousset, L., Abdallah, M., Desfeux, A.S., Etienne, P., Meuriot, F., Hawkesford, M.J., Gombert, J., Avice, J.C., Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability (2009) J. Exp. Bot., 60, pp. 3239-3253
  • Falk, J., Munné-Bosch, S., Tocochromanol functions in plants: antioxidation and beyond (2010) J. Exp. Bot., 61, pp. 1549-1566
  • Fernandez, P., Di Rienzo, J.A., Moschen, S., Dosio, G.A., Aguirrezabal, L.A., Hopp, H.E., Paniego, N., Heinz, R.A., Comparison of predictive methods and biological validation for qPCR reference genes in sunflower leaf senescence transcript analysis (2011) Plant Cell Rep., 30, pp. 63-74
  • Fernandez, P., Moschen, S., Paniego, N., Heinz, R.A., Functional approaches to study leaf senescence in sunflower (2012) Senescence, pp. 69-88. , In (Nagata, T., ed.). Croatia: InTech Open Access Publisher
  • Fernandez, P., Soria, M., Blesa, D., Di Rienzo, J., Moschen, S., Rivarola, M., Clavijo, B.J., Paniego, N., Development, characterization and experimental validation of a cultivated sunflower (Helianthus annuus L.) gene expression oligonucleotide microarray (2012) PLoS One, 7, pp. 1-11
  • Gago, G.M., Almoguera, C., Jordano, J., Gonzalez, D.H., Chan, R.L., Hahb-4, a homeobox-leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower* (2002) Plant Cell Environ., 25, pp. 633-640
  • Gepstein, S., Sabehi, G., Carp, M.-J.-J., Hajouj, T., Nesher, M.F.O., Yariv, I., Dor, C., Bassani, M., Large-scale identification of leaf senescence-associated genes (2003) Plant J., 36, pp. 629-642
  • Gombert, J., Etienne, P., Ourry, A., Le Dily, F., The expression patterns of SAG12/Cab genes reveal the spatial and temporal progression of leaf senescence in Brassica napus L. with sensitivity to the environment (2006) J. Exp. Bot., 57, pp. 1949-1956
  • Graham, I.A., Leaver, C.J., Smith, S.M., Induction of malate synthase gene expression in senescent and detached organs of cucumber (1992) Plant Cell, 4, pp. 349-357
  • Grbic, V., Bleecker, A.B., Ethylene regulates the timing of leaf senescence in Arabidopsis (1995) Plant J., 8, pp. 595-602
  • Gregersen, P.L., Senescence and nutrient remobilization in crop plants (2011) The Molecular and Physiological Basis of Nutrient Use Efficiency in Crops, pp. 83-102. , In (Hawkesford, M.J. and Barraclough, P., eds). Oxford, UK: Wiley-Blackwell
  • Gregersen, P.L., Holm, P.B., Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.) (2007) Plant Biotechnol. J., 5, pp. 192-206
  • Gregersen, P.L., Culetic, A., Boschian, L., Krupinska, K., Plant senescence and crop productivity (2013) Plant Mol. Biol., 82, pp. 603-622
  • Guo, Y., Towards systems biological understanding of leaf senescence (2013) Plant Mol. Biol., 82, pp. 519-528
  • Guo, Y., Gan, S., AtNAP, a NAC family transcription factor, has an important role in leaf senescence (2006) Plant J., 46, pp. 601-612
  • Guo, Y., Gan, S.-S., Convergence and divergence in gene expression profiles induced by leaf senescence and 27 senescence-promoting hormonal, pathological and environmental stress treatments (2012) Plant Cell Environ., 35, pp. 644-655
  • Guo, Y., Cai, Z., Gan, S., Transcriptome of Arabidopsis leaf senescence (2004) Plant Cell Environ., 27, pp. 521-549
  • Gut, H., Matile, P., Apparent induction of key enzymes of the glyoxylic acid cycle in senescent barley leaves (1988) Planta, 176, pp. 548-550
  • He, X.J., Mu, R.L., Cao, W.H., Zhang, Z.G., Zhang, J.S., Chen, S.Y., AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development (2005) Plant J., 44, pp. 903-916
  • Hickman, R., Hill, C., Penfold, C.A., Breeze, E., Bowden, L., Moore, J.D., Zhang, P., Buchanan-Wollaston, V., A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves (2013) Plant J., 75, pp. 26-39
  • Hidema, J., Makino, A., Mae, T., Ojima, K., Photosynthetic characteristics of rice leaves aged under different irradiances from full expansion through senescence (1991) Plant Physiol., 97, pp. 1287-1293
  • Hoeberichts, F.A., van Doorn, W.G., Vorst, O., Hall, R.D., van Wordragen, M.F., Sucrose prevents up-regulation of senescence-associated genes in carnation petals (2007) J. Exp. Bot., 58, pp. 2873-2885
  • Hollmann, J., Gregersen, P.L., Krupinska, K., Identification of predominant genes involved in regulation and execution of senescence-associated nitrogen remobilization in flag leaves of field grown barley (2014) J. Exp. Bot., 65, pp. 3963-3973
  • Hu, R., Qi, G., Kong, Y., Kong, D., Gao, Q., Zhou, G., Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa (2010) BMC Plant Biol., 10, p. 145
  • Janzen, H.H., Bettany, J.R., Sulfur nutrition of rapeseed: I. Influence of fertilizer nitrogen and sulfur rates (1983) Soil Sci. Soc. Am. J., 48, pp. 100-107
  • Jaradat, M.R., Feurtado, J.A., Huang, D., Lu, Y., Cutler, A.J., Multiple roles of the transcription factor AtMYBR1/AtMYB44 in ABA signaling, stress responses, and leaf senescence (2013) BMC Plant Biol., 13, p. 192
  • Jensen, M.K., Lindemose, S., de Masi, F., Reimer, J.J., Nielsen, M., Perera, V., Workman, C.T., Skriver, K., ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana (2013) FEBS Open Bio., 3, pp. 321-327
  • Jukanti, A.K., Heidlebaugh, N.M., Parrott, D.L., Fischer, I.A., McInnerney, K., Fischer, A.M., Comparative transcriptome profiling of near-isogenic barley (Hordeum vulgare) lines differing in the allelic state of a major grain protein content locus identifies genes with possible roles in leaf senescence and nitrogen reallocation (2008) New Phytol., 177, pp. 333-349
  • Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H., Hwang, D., Nam, H.G., Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis (2009) Science, 323, pp. 1053-1057
  • Kim, J.H., Nguyen, N.H., Jeong, C.Y., Nguyen, N.T., Hong, S.-W., Lee, H., Loss of the R2R3 MYB, AtMyb73, causes hyper-induction of the SOS1 and SOS3 genes in response to high salinity in Arabidopsis (2013) J. Plant Physiol., 170, pp. 1461-1465
  • Kim, Y.-S., Sakuraba, Y., Han, S.-H., Yoo, S.-C., Paek, N.-C., Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence (2013) Plant Cell Physiol., 54, pp. 1660-1672
  • Kim, H.J., Hong, S.H., Kim, Y.W., Lee, I.H., Jun, J.H., Phee, B.-K., Rupak, T., Lim, P.O., Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis (2014) J. Exp. Bot., 65, pp. 4023-4036
  • Kiniry, J.R., Blanchet, R., Williams, J.R., Texier, V., Jones, K., Cabelguenne, M., Sunflower simulation using the EPIC and ALMANAC models (1992) Field. Crop. Res., 30, pp. 403-423
  • Kinnersley, A.M., Turano, F.J., Gamma aminobutyric acid (GABA) and plant responses to stress (2000) Crit. Rev. Plant Sci., 19, pp. 479-509
  • Kong, X., Luo, Z., Dong, H., Eneji, A.E., Li, W., Lu, H., Gene expression profiles deciphering leaf senescence variation between early- and late-senescence cotton lines (2013) PLoS One, 8
  • Koyama, T., Nii, H., Mitsuda, N., Ohta, M., Kitajima, S., Ohme-Takagi, M., Sato, F., A regulatory cascade involving class II ETHYLENE RESPONSE FACTOR transcriptional repressors operates in the progression of leaf senescence (2013) Plant Physiol., 162, pp. 991-1005
  • Kusaba, M., Tanaka, A., Tanaka, R., Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence (2013) Photosynth. Res., 117, pp. 221-234
  • Lahdesmaki, P., The amount of gama-aminobutyric acid and the activity of glutamic carboxylase in ageing leaves (1968) Physiol. Plant., 21, pp. 1322-1327
  • Lea, P., Miflin, B., Transport and metabolism of asparagine and other nitrogen compounds within the plant (1980) The Biochemistry of Plants: a Comprehensive Treatise, pp. 569-608. , In (Miflin, B., ed.). New York, NY; London: Academic Press Inc. LTD
  • Lee, R.H., Wang, C.H., Huang, L.T., Chen, S.C., Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes (2001) J. Exp. Bot., 52, pp. 1117-1121
  • Li, Z., Zhao, Y., Liu, X., Peng, J., Guo, H., Luo, J., LSD 2.0: an update of the leaf senescence database (2014) Nucleic Acids Res., 42, pp. D1200-D1205
  • Lim, P.O., Woo, H.R., Nam, H.G., Molecular genetics of leaf senescence in Arabidopsis (2003) Trends Plant Sci., 8, pp. 272-278
  • Lin, J.-F., Wu, S.-H., Molecular events in senescing Arabidopsis leaves (2004) Plant J., 39, pp. 612-628
  • Liu, R., Lü, B., Wang, X., Zhang, C., Zhang, S., Qian, J., Chen, L., Dong, H., Thirty-seven transcription factor genes differentially respond to a harpin protein and affect resistance to the green peach aphid in Arabidopsis (2010) J. Biosci., 35, pp. 435-450
  • Lohman, K.N., Gan, S., John, M.C., Amasino, R.M., Molecular analysis of natural leaf senescence in Arabidopsis thaliana (1994) Physiol. Plant., 92, pp. 322-328
  • Lohse, M., Nagel, A., Herter, T., May, P., Schroda, M., Zrenner, R., Tohge, T., Usadel, B., Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data (2014) Plant Cell Environ., 37, pp. 1250-1258
  • Luedemann, A., Strassburg, K., Erban, A., Kopka, J., TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments (2008) Bioinformatics, 24, pp. 732-737
  • Manavella, P.A., Arce, A.L., Dezar, C.A., Bitton, F., Renou, J.-P., Crespi, M., Chan, R.L., Cross-talk between ethylene and drought signalling pathways is mediated by the sunflower Hahb-4 transcription factor (2006) Plant J., 48, pp. 125-137
  • Manavella, P.A., Dezar, C.A., Ariel, F.D., Drincovich, M.F., Chan, R.L., The sunflower HD-Zip transcription factor HAHB4 is up-regulated in darkness, reducing the transcription of photosynthesis-related genes (2008) J. Exp. Bot., 59, pp. 3143-3155
  • Manavella, P.A., Dezar, C.A., Bonaventure, G., Baldwin, I.T., Chan, R.L., HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses (2008) Plant J., 56, pp. 376-388
  • Martin, A., Lee, J., Kichey, T., Gerentes, D., Zivy, M., Tatout, C., Dubois, F., Hirel, B., Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production (2006) Plant Cell, 18, pp. 3252-3274
  • Martínez, D.E., Costa, M.L., Gomez, F.M., Otegui, M.S., Guiamet, J.J., "Senescence-associated vacuoles" are involved in the degradation of chloroplast proteins in tobacco leaves (2008) Plant J., 56, pp. 196-206
  • Masclaux, C., Valadier, M.H., Brugiere, N., Morot-Gaudry, J.F., Hirel, B., Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence (2000) Planta, 211, pp. 510-518
  • Masclaux-Daubresse, C., Carrayol, E., Valadier, M.-H., The two nitrogen mobilisation- and senescence-associated GS1 and GDH genes are controlled by C and N metabolites (2005) Planta, 221, pp. 580-588
  • Matallana-Ramirez, L.P., Rauf, M., Farage-Barhom, S., Dortay, H., Xue, G.-P., Dröge-Laser, W., Lers, A., Mueller-Roeber, B., NAC transcription factor ORE1 and senescence-induced BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade in Arabidopsis (2013) Mol Plant, 1, pp. 1-34
  • McIntyre, G.I., The role of nitrate in the osmotic and nutritional control of plant development (1997) Aust. J. Plant Physiol., 24, p. 103
  • Miao, Y., Smykowski, A., Zentgraf, U., A novel upstream regulator of WRKY53 transcription during leaf senescence in Arabidopsis thaliana (2008) Plant Biol (Stuttg), 10, pp. 110-120
  • Molina-Torres, J., Martinez, M.L., Tocopherols and leaf age in Xanthium strumarium L (1991) New Phytol., 118, pp. 95-99
  • Montaner, D., Dopazo, J., Multidimensional gene set analysis of genomic data (2010) PLoS One, 5
  • Moschen, S., Bengoa Luoni, S., Paniego, N.B., Hopp, H.E., Dosio, G.A.A., Fernandez, P., Heinz, R.A., Identification of candidate genes associated with leaf senescence in cultivated sunflower (Helianthus annuus L.) (2014) PLoS One, 9
  • Nooden, L.D., Whole plant senescence (1988) Senescence and Aging in Plants, pp. 392-439. , In (L. D, Nooden and A. C., Leopold, eds). San Diego, CA: Academic Press
  • Nuruzzaman, M., Manimekalai, R., Sharoni, A.M., Satoh, K., Kondoh, H., Ooka, H., Kikuchi, S., Genome-wide analysis of NAC transcription factor family in rice (2010) Gene, 465, pp. 30-44
  • Obata, T., Fernie, A.R., The use of metabolomics to dissect plant responses to abiotic stresses (2012) Cell. Mol. Life Sci., 69, pp. 3225-3243
  • Pageau, K., Reisdorf-Cren, M., Morot-Gaudry, J.-F., Masclaux-Daubresse, C., The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicoti (2006) J. Exp. Bot., 57, pp. 547-557
  • Parrott, D.L., McInnerney, K., Feller, U., Fischer, A.M., Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes (2007) New Phytol., 176, pp. 56-69
  • Parrott, D.L., Martin, J.M., Fischer, A.M., Analysis of barley (Hordeum vulgare) leaf senescence and protease gene expression: a family C1A cysteine protease is specifically induced under conditions characterized by high carbohydrate, but low to moderate nitrogen levels (2010) New Phytol., 187, pp. 313-331
  • Peluffo, L., Lia, V., Troglia, C., Maringolo, C., Norma, P., Escande, A., Esteban Hopp, H., Carrari, F., Metabolic profiles of sunflower genotypes with contrasting response to Sclerotinia sclerotiorum infection (2010) Phytochemistry, 71, pp. 70-80
  • Pérez-Rodríguez, P., Riaño-Pachón, D.M., Corrêa, L.G.G., Rensing, S.A., Kersten, B., Mueller-Roeber, B., PlnTFDB: updated content and new features of the plant transcription factor database (2010) Nucleic Acids Res., 38, pp. D822-D827
  • Pic, E., de la Serve, T.B., Tardieu, F., Turc, O., Leaf senescence induced by mild water deficit follows the same sequence of macroscopic, biochemical, and molecular events as monocarpic senescence in pea (2002) Plant Physiol., 128, pp. 236-246
  • Pichersky, E., Noel, J.P., Dudareva, N., Biosynthesis of plant volatiles: nature's diversity and ingenuity (2006) Science, 311, pp. 808-811
  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., (2012), nlme: linear and nonlinear mixed effects models. R package; Quadrana, L., Almeida, J., Otaiza, S.N., Duffy, T., Corrêa da Silva, J.V., de Godoy, F., Asís, R., Rossi, M., Transcriptional regulation of tocopherol biosynthesis in tomato (2013) Plant Mol. Biol., 81, pp. 309-325
  • Quirino, B.F., Noh, Y.S., Himelblau, E., Amasino, R.M., Molecular aspects of leaf senescence (2000) Trends Plant Sci., 5, pp. 278-282
  • Quirino, B.F., Reiter, W.-D., Amasino, R.D., One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated (2001) Plant Mol. Biol., 46, pp. 447-457
  • (2012) R: A Language and Environment for Statistical Computing, , Vienna, Austria: R Foundation for Statistical Computing
  • Radwanski, E.R., Last, R.L., Tryptophan biosynthesis and metabolism: biochemical and molecular genetics (1995) Plant Cell, 7, pp. 921-934
  • Rauf, M., Arif, M., Dortay, H., Matallana-Ramírez, L.P., Waters, M.T., Gil Nam, H., Lim, P.-O., Balazadeh, S., ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription (2013) EMBO Rep., 14, pp. 382-388
  • Rise, M., Cojocaru, M., Gottlieb, H.E., Goldschmidt, E.E., Accumulation of alpha-Tocopherol in Senescing Organs as Related to Chlorophyll Degradation (1989) Plant Physiol., 89, pp. 1028-1030
  • Roberts, M.R., Does GABA act as a signal in plants?: hints from molecular studies (2007) Plant Signal. Behav., 2, pp. 408-409
  • Roberts, I.N., Caputo, C., Criado, M.V., Funk, C., Senescence-associated proteases in plants (2012) Physiol. Plant., 145, pp. 130-139
  • Roessner-Tunali, U., Hegemann, B., Lytovchenko, A., Carrari, F., Bruedigam, C., Granot, D., Fernie, A.R., Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development (2003) Plant Physiol., 133, pp. 84-99
  • Roitsch, T., González, M.-C., Function and regulation of plant invertases: sweet sensations (2004) Trends Plant Sci., 9, pp. 606-613
  • Rozen, S., Skaletsky, H.J., Primer3 on the WWW for general users and for biologist programmers (2000) Methods Mol. Biol., 132, pp. 365-386
  • Rushton, D.L., Tripathi, P., Rabara, R.C., Lin, J., Ringler, P., Boken, A.K., Langum, T.J., Rushton, P.J., WRKY transcription factors: key components in abscisic acid signalling (2012) Plant Biotechnol. J., 10, pp. 2-11
  • Ruuska, S.A., Lewis, D.C., Kennedy, G., Furbank, R.T., Jenkins, C.L.D., Tabe, L.M., Large scale transcriptome analysis of the effects of nitrogen nutrition on accumulation of stem carbohydrate reserves in reproductive stage wheat (2008) Plant Mol. Biol., 66, pp. 15-32
  • Sadras, V.O., Echarte, L., Andrade, F.H., Profiles of leaf senescence during reproductive growth of sunflower and maize (2000) Ann. Bot., 85, pp. 187-195
  • Sadras, V.O., Quiroz, F., Echarte, L., Escande, A., Pereyra, V.R., Effect of Verticillium dahliae on photosynthesis, leaf expansion and senescence of field-grown sunflower (2000) Ann. Bot., 86, pp. 1007-1015
  • Scherer, H.W., Sulphur in crop production-invited paper (2001) Eur. J. Agron., 14, pp. 81-111
  • Schiltz, S., Gallardo, K., Huart, M., Negroni, L., Sommerer, N., Burstin, J., Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling (2004) Plant Physiol., 135, pp. 2241-2260
  • Sekhon, R.S., Childs, K.L., Santoro, N., Foster, C.E., Buell, C.R., de Leon, N., Kaeppler, S.M., Transcriptional and metabolic analysis of senescence induced by preventing pollination in maize (2012) Plant Physiol., 159, pp. 1730-1744
  • Shan, W., Kuang, J., Chen, L., Xie, H., Peng, H., Xiao, Y., Li, X., Lu, W., Molecular characterization of banana NAC transcription factors and their interactions with ethylene signalling component EIL during fruit ripening (2012) J. Exp. Bot., 63, pp. 5171-5187
  • Smeekens, S., Ma, J., Hanson, J., Rolland, F., Sugar signals and molecular networks controlling plant growth (2010) Curr. Opin. Plant Biol., 13, pp. 274-279
  • Smyth, G., Limma: linear models for microarray data (2005) Bioinformatics and Computational Biology Solutions using R and Bioconductor, pp. 397-420. , In (Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W., eds). New York: Springer
  • Tabuchi, M., Abiko, T., Yamaya, T., Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.) (2007) J. Exp. Bot., 58, pp. 2319-2327
  • Thimm, O., Blasing, O., Gibon, Y., Nagel, A., Meyer, S., Kruger, P., Selbig, J., Müller, L.A., MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes (2004) Plant J., 37, pp. 914-939
  • Uauy, C., Distelfeld, A., Fahima, T., Blechl, A., Dubcovsky, J., A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat (2006) Science, 314, pp. 1298-1301
  • Ulker, B., Shahid Mukhtar, M., Somssich, I.E., The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways (2007) Planta, 226, pp. 125-137
  • Urquhart, A.A., Joy, K.W., Use of Phloem exudate technique in the study of amino Acid transport in pea plants (1981) Plant Physiol., 68, pp. 750-754
  • Wang, Z., Dane, F., NAC (NAM/ATAF/CUC) transcription factors in different stresses and their signaling pathway (2013) Acta Physiologiae Plantarum, 35 (5), pp. 1397-1408
  • Wang, X., Basnayake, B.M.V.S., Zhang, H., Li, G., Li, W., Virk, N., Mengiste, T., Song, F., The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens (2009) Mol. Plant Microbe Interact., 22, pp. 1227-1238
  • Watanabe, M., Balazadeh, S., Tohge, T., Erban, A., Giavalisco, P., Kopka, J., Mueller-Roeber, B., Hoefgen, R., Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis (2013) Plant Physiol., 162, pp. 1290-1310
  • Wingler, A., Von Schaewen, A., Leegood, R.C., Lea, P.L., Quick, P.W., Regulation of leaf senescence by cytokinin, sugars, and light (1998) Plant Physiol., 116, pp. 329-335
  • Wingler, A., Purdy, S., MacLean, J.A., Pourtau, N., The role of sugars in integrating environmental signals during the regulation of leaf senescence (2006) J. Exp. Bot., 57, pp. 391-399
  • Wingler, A., Masclaux-Daubresse, C., Fischer, A.M., Sugars, senescence, and ageing in plants and heterotrophic organisms (2009) J. Exp. Bot., 60, pp. 1063-1066
  • Wingler, A., Delatte, T., O'Hara, L., Primavesi, L., Jhurreea, D., Paul, M., Schluepmann, H., Trehalose 6-Phosphate is required for the onset of leaf senescence associated with high carbon availability (2012) Plant Physiol., 158, pp. 1241-1251
  • Yoshida, S., Molecular regulation of leaf senescence (2003) Curr. Opin. Plant Biol., 6 (1), pp. 79-84
  • Zhang, X., Ju, H.-W., Chung, M.-S., Huang, P., Ahn, S.-J., Kim, C.S., The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis (2011) Plant Cell Physiol., 52, pp. 138-148
  • Zhang, W.Y., Xu, Y.C., Li, W.L., Yang, L., Yue, X., Zhang, X.S., Zhao, X.Y., Transcriptional analyses of natural leaf senescence in maize (2014) PLoS One, 9
  • Zhou, X., Jiang, Y., Yu, D., WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis (2011) Mol. Cells, 31, pp. 303-313

Citas:

---------- APA ----------
Moschen, S., Bengoa Luoni, S., Di Rienzo, J.A., Caro, M.del.P., Tohge, T., Watanabe, M., Hollmann, J.,..., Heinz, R.A. (2016) . Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower. Plant Biotechnology Journal, 14(2), 719-734.
http://dx.doi.org/10.1111/pbi.12422
---------- CHICAGO ----------
Moschen, S., Bengoa Luoni, S., Di Rienzo, J.A., Caro, M.del.P., Tohge, T., Watanabe, M., et al. "Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower" . Plant Biotechnology Journal 14, no. 2 (2016) : 719-734.
http://dx.doi.org/10.1111/pbi.12422
---------- MLA ----------
Moschen, S., Bengoa Luoni, S., Di Rienzo, J.A., Caro, M.del.P., Tohge, T., Watanabe, M., et al. "Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower" . Plant Biotechnology Journal, vol. 14, no. 2, 2016, pp. 719-734.
http://dx.doi.org/10.1111/pbi.12422
---------- VANCOUVER ----------
Moschen, S., Bengoa Luoni, S., Di Rienzo, J.A., Caro, M.del.P., Tohge, T., Watanabe, M., et al. Integrating transcriptomic and metabolomic analysis to understand natural leaf senescence in sunflower. Plant Biotechnol. J. 2016;14(2):719-734.
http://dx.doi.org/10.1111/pbi.12422