Transcriptional and Metabolic Analysis of Senescence Induced by Preventing Pollination in Maize1[W][OA]

Transcriptional and metabolic changes were evaluated during senescence induced by preventing pollination in the B73 genotype of maize (Zea mays). Accumulation of free glucose and starch and loss of chlorophyll in leaf was manifested early at 12 d after anthesis (DAA), while global transcriptional and phenotypic changes were evident only at 24 DAA. Internodes exhibited major transcriptomic changes only at 30 DAA. Overlaying expression data onto metabolic pathways revealed involvement of many novel pathways, including those involved in cell wall biosynthesis. To investigate the overlap between induced and natural senescence, transcriptional data from induced senescence in maize was compared with that reported for Arabidopsis (Arabidopsis thaliana) undergoing natural and sugar-induced senescence. Notable similarities with natural senescence in Arabidopsis included up-regulation of senescence-associated genes (SAGs), ethylene and jasmonic acid biosynthetic genes, APETALA2, ethylene-responsive element binding protein, and no apical meristem transcription factors. However, differences from natural senescence were highlighted by unaltered expression of a subset of the SAGs, and cytokinin, abscisic acid, and salicylic acid biosynthesis genes. Key genes up-regulated during sugar-induced senescence in Arabidopsis, including a cysteine protease (SAG12) and three flavonoid biosynthesis genes (PRODUCTION OF ANTHOCYANIN PIGMENT1 (PAP1), PAP2, and LEUCOANTHOCYANIDIN DIOXYGENASE), were also induced, suggesting similarities in senescence induced by pollination prevention and sugar application. Coexpression analysis revealed networks involving known senescence-related genes and novel candidates; 82 of these were shared between leaf and internode networks, highlighting similarities in induced senescence in these tissues. Insights from this study will be valuable in systems biology of senescence in maize and other grasses.

[1]  Julie A. Dickerson,et al.  PLEXdb: gene expression resources for plants and plant pathogens , 2011, Nucleic Acids Res..

[2]  Chung-Mo Park,et al.  The Arabidopsis NAC Transcription Factor VNI2 Integrates Abscisic Acid Signals into Leaf Senescence via the COR/RD Genes[W] , 2011, Plant Cell.

[3]  T. Demura,et al.  VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. , 2011, The Plant journal : for cell and molecular biology.

[4]  R. Sekhon,et al.  Genome-wide atlas of transcription during maize development. , 2011, The Plant journal : for cell and molecular biology.

[5]  Zhonghai Li,et al.  LSD: a leaf senescence database , 2010, Nucleic Acids Res..

[6]  Christopher A. Penfold,et al.  High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation , 2011 .

[7]  K. Keegstra,et al.  Arabidopsis mannan synthase CSLA9 and glucan synthase CSLC4 have opposite orientations in the Golgi membrane. , 2010, The Plant journal : for cell and molecular biology.

[8]  H. Scheller,et al.  An Integrative Approach to the Identification of Arabidopsis and Rice Genes Involved in Xylan and Secondary Wall Development , 2010, PloS one.

[9]  H. Fukuda,et al.  Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation[C][W] , 2010, Plant Cell.

[10]  L. Hennig,et al.  Arabidopsis RETINOBLASTOMA-RELATED Is Required for Stem Cell Maintenance, Cell Differentiation, and Lateral Organ Production[W][OA] , 2010, Plant Cell.

[11]  K. Dietz,et al.  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.

[12]  Markus Pauly,et al.  Comprehensive Compositional Analysis of Plant Cell Walls (Lignocellulosic biomass) Part I: Lignin , 2010, Journal of visualized experiments : JoVE.

[13]  M. Pauly,et al.  A High-Throughput Platform for Screening Milligram Quantities of Plant Biomass for Lignocellulose Digestibility , 2010, BioEnergy Research.

[14]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[15]  S. Reinbothe,et al.  Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence , 2009, The FEBS journal.

[16]  S. Hörtensteiner.  Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. , 2009, Trends in plant science.

[17]  A. Fischer,et al.  Sugars, senescence, and ageing in plants and heterotrophic organisms. , 2009, Journal of experimental botany.

[18]  Daehee Hwang,et al.  Trifurcate Feed-Forward Regulation of Age-Dependent Cell Death Involving miR164 in Arabidopsis , 2009, Science.

[19]  Steve Horvath,et al.  WGCNA: an R package for weighted correlation network analysis , 2008, BMC Bioinformatics.

[20]  D. Janies,et al.  GRASSIUS: A Platform for Comparative Regulatory Genomics across the Grasses1[W][OA] , 2008, Plant Physiology.

[21]  R. Quatrano,et al.  Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor1[W][OA] , 2008, Plant Physiology.

[22]  T. Roitsch,et al.  Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. , 2008, Plant biology.

[23]  P. Perata,et al.  Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. , 2008, The New phytologist.

[24]  S. Shigeoka,et al.  Galactinol and Raffinose Constitute a Novel Function to Protect Plants from Oxidative Damage1[W][OA] , 2008, Plant Physiology.

[25]  P. Schnable,et al.  The maize (Zea mays L.) roothairless3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield , 2008, The Plant journal : for cell and molecular biology.

[26]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): gene structure and function annotation , 2007, Nucleic Acids Res..

[27]  W. G. van Doorn.  Is the onset of senescence in leaf cells of intact plants due to low or high sugar levels? , 2008, Journal of experimental botany.

[28]  Peter Langfelder,et al.  Eigengene networks for studying the relationships between co-expression modules , 2007, BMC Systems Biology.

[29]  A. Fischer,et al.  Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. , 2007, The New phytologist.

[30]  P. Beyer,et al.  Transcription Factor RAP2.2 and Its Interacting Partner SINAT2: Stable Elements in the Carotenogenesis of Arabidopsis Leaves1[W] , 2007, Plant Physiology.

[31]  John A. Hamilton,et al.  The TIGR Rice Genome Annotation Resource: improvements and new features , 2006, Nucleic Acids Res..

[32]  H. Nam,et al.  Leaf senescence. , 2007, Annual review of plant biology.

[33]  P. Beyer,et al.  Transcription Factor RAP 2 . 2 and Its Interacting Partner SINAT 2 : Stable Elements in the Carotenogenesis of Arabidopsis Leaves 1 [ W ] , 2007 .

[34]  T. Demura,et al.  SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis[W] , 2006, The Plant Cell Online.

[35]  U. Flügge,et al.  Transcription Analysis of Arabidopsis Membrane Transporters and Hormone Pathways during Developmental and Induced Leaf Senescence1[W] , 2006, Plant Physiology.

[36]  E. Pelzer,et al.  Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis , 2006, Planta.

[37]  V. Shuvalov,et al.  Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. , 2006, Journal of experimental botany.

[38]  R. Liechti,et al.  Jasmonate Biochemical Pathway , 2006, Science's STKE.

[39]  P. Perata,et al.  Sucrose-Specific Induction of the Anthocyanin Biosynthetic Pathway in Arabidopsis[W] , 2005, Plant Physiology.

[40]  S. Horvath,et al.  A General Framework for Weighted Gene Co-Expression Network Analysis , 2005, Statistical applications in genetics and molecular biology.

[41]  Joachim Selbig,et al.  Extension of the Visualization Tool MapMan to Allow Statistical Analysis of Arrays, Display of Coresponding Genes, and Comparison with Known Responses1 , 2005, Plant Physiology.

[42]  C. Masclaux-Daubresse,et al.  Characterization of Markers to Determine the Extent and Variability of Leaf Senescence in Arabidopsis. A Metabolic Profiling Approach1 , 2005, Plant Physiology.

[43]  Vicky Buchanan-Wollaston,et al.  Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[44]  H. Nam,et al.  The molecular and genetic control of leaf senescence and longevity in Arabidopsis. , 2005, Current topics in developmental biology.

[45]  S. Gan,et al.  Leaf senescence: signals, execution, and regulation. , 2005, Current topics in developmental biology.

[46]  T. Roitsch,et al.  Function and regulation of plant invertases: sweet sensations. , 2004, Trends in plant science.

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

[48]  O. Zakhleniuk,et al.  Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. , 2004, Journal of experimental botany.

[49]  P. Mendes,et al.  myo-Inositol Oxygenase Offers a Possible Entry Point into Plant Ascorbate Biosynthesis1 , 2004, Plant Physiology.

[50]  B. Quirino,et al.  One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated , 2001, Plant Molecular Biology.

[51]  F. Meins,et al.  Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I β-1,3-glucanase during tobacco seed germination , 1998, Plant Molecular Biology.

[52]  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.

[53]  R. Liechti,et al.  The Jasmonate Biochemical Pathway , 2003, Science's STKE.

[54]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[55]  Andrea Pitzschke,et al.  Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato - amplification in wound signalling. , 2003, The Plant journal : for cell and molecular biology.

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

[57]  K. Dietz.  Redox control, redox signaling, and redox homeostasis in plant cells. , 2003, International review of cytology.

[58]  W. Reiter.  Biosynthesis and properties of the plant cell wall. , 2002, Current opinion in plant biology.

[59]  E. Nambara,et al.  A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions , 2002, The Plant Cell Online.

[60]  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.

[61]  R. Amasino,et al.  Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence , 2001 .

[62]  M. Sussman,et al.  Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[63]  R. Amasino,et al.  Molecular aspects of leaf senescence. , 2000, Trends in plant science.

[64]  S. Huber,et al.  Regulation of Sucrose Metabolism in Higher Plants: Localization and regulation of Activity of Key Enzymes , 2000, Critical reviews in biochemistry and molecular biology.

[65]  J. Miller,et al.  Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. , 1999, Plant physiology.

[66]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Samantha Vernhettes,et al.  A plasma membrane‐bound putative endo‐1,4‐β‐D‐glucanase is required for normal wall assembly and cell elongation in Arabidopsis , 1998, The EMBO journal.

[68]  J. Thompson,et al.  Lipid metabolism during plant senescence. , 1998, Progress in lipid research.

[69]  R. Amasino,et al.  Molecular analysis of natural leaf senescence in Arabidopsis thaliana , 1994 .

[70]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[71]  M. Estelle,et al.  Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana , 1988, Science.

[72]  R. Khanna-Chopra,et al.  Regulation of Leaf Senescence by Reproductive Sink Intensity in Cowpea (Vigna Unguiculata L. Walp) , 1988 .

[73]  M. Motto,et al.  Genotype-dependent leaf senescence in maize : inheritance and effects of pollination-prevention. , 1987, Plant physiology.

[74]  S. Crafts-Brandner,et al.  Sink removal and leaf senescence in soybean : cultivar effects. , 1987, Plant physiology.

[75]  F. Below,et al.  Effect of head removal on leaf senescence of sunflower. , 1987, Plant physiology.

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

[77]  S. Mandal,et al.  Monocarpic senescence in wheat: Influence of sterile glumes and ear , 1986 .

[78]  F. Below,et al.  Effects of pod removal on metabolism and senescence of nodulating and nonnodulating soybean isolines: I. Metabolic constituents. , 1984, Plant physiology.

[79]  F. Below,et al.  Differential Senescence of Maize Hybrids following Ear Removal : II. Selected Leaf. , 1984, Plant physiology.

[80]  F. Below,et al.  The effects of ear removal on senescence and metabolism of maize. , 1981, Plant physiology.

[81]  C. Brady,et al.  Assimilate Source-Sink Relationships in Capsicum annuum L. II. Effects of Fruiting and Defloration on the Photosynthetic Capacity and Senescence of the Leaves , 1977 .