Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis.

An analysis of changes in global gene expression patterns during developmental leaf senescence in Arabidopsis has identified more than 800 genes that show a reproducible increase in transcript abundance. This extensive change illustrates the dramatic alterations in cell metabolism that underpin the developmental transition from a photosynthetically active leaf to a senescing organ which functions as a source of mobilizable nutrients. Comparison of changes in gene expression patterns during natural leaf senescence with those identified, when senescence is artificially induced in leaves induced to senesce by darkness or during sucrose starvation-induced senescence in cell suspension cultures, has shown not only similarities but also considerable differences. The data suggest that alternative pathways for essential metabolic processes such as nitrogen mobilization are used in different senescent systems. Gene expression patterns in the senescent cell suspension cultures are more similar to those for dark-induced senescence and this may be a consequence of sugar starvation in both tissues. Gene expression analysis in senescing leaves of plant lines defective in signalling pathways involving salicylic acid (SA), jasmonic acid (JA) and ethylene has shown that these three pathways are all required for expression of many genes during developmental senescence. The JA/ethylene pathways also appear to operate in regulating gene expression in dark-induced and cell suspension senescence whereas the SA pathway is not involved. The importance of the SA pathway in the senescence process is illustrated by the discovery that developmental leaf senescence, but not dark-induced senescence, is delayed in plants defective in the SA pathway.

[1]  Leslie Friedrich,et al.  Requirement of Salicylic Acid for the Induction of Systemic Acquired Resistance , 1993, Science.

[2]  R. Amasino,et al.  A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment , 1998, Plant Molecular Biology.

[3]  David W. Lee,et al.  Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. , 2001, Plant physiology.

[4]  D. Xie,et al.  COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. , 1998, Science.

[5]  G. Coruzzi,et al.  Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. , 1995, The Plant cell.

[6]  J. Kieber,et al.  Cytokinin Signaling in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010444. , 2002, The Plant Cell Online.

[7]  Masaki Ito,et al.  Leucine and its keto acid enhance the coordinated expression of genes for branched‐chain amino acid catabolism in Arabidopsis under sugar starvation , 2001, FEBS letters.

[8]  Lijun Liu,et al.  Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling , 2003 .

[9]  R. Vierstra,et al.  The ubiquitin 26S proteasome proteolytic pathway. , 2004, Annual review of plant biology.

[10]  Anders F. Andersson,et al.  A transcriptional timetable of autumn senescence , 2004, Genome Biology.

[11]  Shu-Hsing Wu,et al.  Molecular events in senescing Arabidopsis leaves. , 2004, The Plant journal : for cell and molecular biology.

[12]  Stefan Hörtensteiner,et al.  Nitrogen metabolism and remobilization during senescence. , 2002, Journal of experimental botany.

[13]  A. Bleecker,et al.  Ethylene regulates the timing of leaf senescence in Arabidopsis , 1995 .

[14]  J. Glazebrook,et al.  Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. , 2000, Molecular plant-microbe interactions : MPMI.

[15]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[16]  P. Eastmond,et al.  Pathways of straight and branched chain fatty acid catabolism in higher plants. , 2002, Progress in lipid research.

[17]  S. Hörtensteiner The loss of green color during chlorophyll degradation—a prerequisite to prevent cell death? , 2004, Planta.

[18]  K. Raghothama,et al.  Phosphate transporters from the higher plant Arabidopsis thaliana. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  H. Nam,et al.  The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. , 2004, Plant & cell physiology.

[20]  D. Shibata,et al.  Leaf Senescence and Starvation-Induced Chlorosis Are Accelerated by the Disruption of an Arabidopsis Autophagy Gene1 , 2002, Plant Physiology.

[21]  M. Hamberg,et al.  Involvement of the Arabidopsis alpha-DOX1 fatty acid dioxygenase in protection against oxidative stress and cell death. , 2002, The Plant journal : for cell and molecular biology.

[22]  J. Ecker,et al.  EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. , 1999, Science.

[23]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[24]  S. Gan,et al.  Evidence Supporting a Role of Jasmonic Acid in Arabidopsis Leaf Senescence1 , 2002, Plant Physiology.

[25]  N. Chua,et al.  Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[26]  Jonathan D. G. Jones,et al.  Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling , 2000 .

[27]  Shoshi Kikuchi,et al.  Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. , 2003, DNA research : an international journal for rapid publication of reports on genes and genomes.

[28]  Sang-Jin Kim,et al.  Transcriptome Profiling of the Response of Arabidopsis Suspension Culture Cells to Suc Starvation1[w] , 2004, Plant Physiology.

[29]  E. Harrison,et al.  The molecular analysis of leaf senescence--a genomics approach. , 2002, Plant biotechnology journal.

[30]  L. Mcintosh,et al.  The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Hong Gil Nam,et al.  ORE9, an F-Box Protein That Regulates Leaf Senescence in Arabidopsis , 2001, The Plant Cell Online.

[32]  H. Fromm,et al.  GABA in plants: just a metabolite? , 2004, Trends in plant science.

[33]  B. Winkel-Shirley,et al.  Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. , 2001, Plant physiology.

[34]  W. Doorn Is Petal Senescence Due to Sugar Starvation , 2004 .

[35]  D. Bouchez,et al.  Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Benschop,et al.  The role of the alternative oxidase in stabilizing the in vivo reduction state of the ubiquinone pool and the activation state of the alternative oxidase , 1998, Plant physiology.

[37]  A. Jones,et al.  Programmed cell death in development and defense. , 2001, Plant physiology.

[38]  Jörg Durner,et al.  Salicylic acid and disease resistance in plants , 1997 .

[39]  Kazuo Shinozaki,et al.  A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. , 2004, The Plant journal : for cell and molecular biology.

[40]  D. Callaham,et al.  Increases in Cytosolic Ca2+ in Parsley Mesophyll Cells Correlate with Leaf Senescence , 1997, Plant physiology.

[41]  Shimon Gepstein,et al.  Large-scale identification of leaf senescence-associated genes. , 2003, The Plant journal : for cell and molecular biology.

[42]  F. Badeck,et al.  Metabolic Origin of Carbon Isotope Composition of Leaf Dark-Respired CO2 in French Bean1 , 2003, Plant Physiology.

[43]  H. Lichtenthaler CHLOROPHYLL AND CAROTENOIDS: PIGMENTS OF PHOTOSYNTHETIC BIOMEMBRANES , 1987 .

[44]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[45]  S. Merlot,et al.  The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. , 1997, The Plant cell.

[46]  L. Sweetlove,et al.  A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[47]  K. Apel,et al.  Differences in gene expression between natural and artificially induced leaf senescence , 2004, Planta.

[48]  A. V. Van Dijken,et al.  Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  V. Portnoy,et al.  The early light-induced protein is also produced during leaf senescence of Nicotiana tabacum , 2001, Planta.

[50]  J. Gaudillère,et al.  Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to Light/Dark cycles and to extended darkness , 1998, Plant physiology.

[51]  Y. Abiko [57] Pantothenic acid and coenzyme A: Phosphopantothenoylcysteine synthetase from rat liver (pantothenate 4′-phosphate:l-cysteine ligase, EC 6.3.2.5) , 1970 .

[52]  Ruey-Hua Lee,et al.  Programmed cell death during rice leaf senescence is nonapoptotic. , 2002, The New phytologist.

[53]  Nicolae Moise,et al.  Early light-induced proteins protect Arabidopsis from photooxidative stress , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Y. Kamiya,et al.  Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. , 2000, The Plant journal : for cell and molecular biology.

[55]  S. Rhee,et al.  MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. , 2004, The Plant journal : for cell and molecular biology.

[56]  P. Eastmond,et al.  Is trehalose-6-phosphate a regulator of sugar metabolism in plants? , 2003, Journal of experimental botany.

[57]  M. Haruta,et al.  Rapid Alkalinization Factors in Poplar Cell Cultures. Peptide Isolation, cDNA Cloning, and Differential Expression in Leaves and Methyl Jasmonate-Treated Cells1 , 2003, Plant Physiology.

[58]  G. Sarath,et al.  The role of acid phosphatases in plant phosphorus metabolism , 1994 .

[59]  S. Gan,et al.  Transcriptome of Arabidopsis leaf senescence , 2004 .

[60]  J. Falk,et al.  Constitutive overexpression of barley 4‐hydroxyphenylpyruvate dioxygenase in tobacco results in elevation of the vitamin E content in seeds but not in leaves 1 , 2003, FEBS letters.

[61]  S. Kay,et al.  Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. , 2000, Science.

[62]  R. Amasino,et al.  Inhibition of Leaf Senescence by Autoregulated Production of Cytokinin , 1995, Science.

[63]  L. Willmitzer,et al.  Improved method for the isolation of RNA from plant tissues. , 1987, Analytical biochemistry.

[64]  M. Hamberg,et al.  alpha-oxidation of fatty acids in higher plants. Identification of a pathogen-inducible oxygenase (piox) as an alpha-dioxygenase and biosynthesis of 2-hydroperoxylinolenic acid. , 1999, The Journal of biological chemistry.

[65]  J. Schjoerring,et al.  Post-translational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. , 2000, The Plant journal : for cell and molecular biology.

[66]  K. Morris,et al.  Salicylic acid has a role in regulating gene expression during leaf senescence. , 2000, The Plant journal : for cell and molecular biology.

[67]  Jiman Kang,et al.  The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[68]  M. Roca,et al.  Chlorophyll breakdown: Pheophorbide a oxygenase is a Rieske-type iron–sulfur protein, encoded by the accelerated cell death 1 gene , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[69]  R. Vierstra,et al.  The APG8/12-activating Enzyme APG7 Is Required for Proper Nutrient Recycling and Senescence in Arabidopsis thaliana * , 2002, The Journal of Biological Chemistry.

[70]  H. Nam,et al.  A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence , 1996, Plant Molecular Biology.