Specification of Cortical Parenchyma and Stele of Maize Primary Roots by Asymmetric Levels of Auxin, Cytokinin, and Cytokinin-Regulated Proteins1[C][W][OA]

In transverse orientation, maize (Zea mays) roots are composed of a central stele that is embedded in multiple layers of cortical parenchyma. The stele functions in the transport of water, nutrients, and photosynthates, while the cortical parenchyma fulfills metabolic functions that are not very well characterized. To better understand the molecular functions of these root tissues, protein- and phytohormone-profiling experiments were conducted. Two-dimensional gel electrophoresis combined with electrospray ionization tandem mass spectrometry identified 59 proteins that were preferentially accumulated in the cortical parenchyma and 11 stele-specific proteins. Hormone profiling revealed preferential accumulation of indole acetic acid and its conjugate indole acetic acid-aspartate in the stele and predominant localization of the cytokinin cis-zeatin, its precursor cis-zeatin riboside, and its conjugate cis-zeatin O-glucoside in the cortical parenchyma. A root-specific β-glucosidase that functions in the hydrolysis of cis-zeatin O-glucoside was preferentially accumulated in the cortical parenchyma. Similarly, four enzymes involved in ammonium assimilation that are regulated by cytokinin were preferentially accumulated in the cortical parenchyma. The antagonistic distribution of auxin and cytokinin in the stele and cortical parenchyma, together with the cortical parenchyma-specific accumulation of cytokinin-regulated proteins, suggest a molecular framework that specifies the function of these root tissues that also play a role in the formation of lateral roots from pericycle and endodermis cells.

[1]  Mariusz Kowalczyk,et al.  An Auxin Gradient and Maximum in the Arabidopsis Root Apex Shown by High-Resolution Cell-Specific Analysis of IAA Distribution and Synthesis[W] , 2009, The Plant Cell Online.

[2]  Jan Petrásek,et al.  Cytokinin regulates root meristem activity via modulation of the polar auxin transport , 2009, Proceedings of the National Academy of Sciences.

[3]  Jaroslava Dubová,et al.  Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux , 2009, Proceedings of the National Academy of Sciences.

[4]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[5]  H. Piepho,et al.  Analysis of nonadditive protein accumulation in young primary roots of a maize (Zea mays L.) F1‐hybrid compared to its parental inbred lines , 2008, Proteomics.

[6]  J. Sheen,et al.  Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis , 2008, Nature.

[7]  Tom Beeckman,et al.  Cytokinins Act Directly on Lateral Root Founder Cells to Inhibit Root Initiation[W] , 2007, The Plant Cell Online.

[8]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[9]  H. Nguyen,et al.  Cell Wall Proteome in the Maize Primary Root Elongation Zone. II. Region-Specific Changes in Water Soluble and Lightly Ionically Bound Proteins under Water Deficit1[W][OA] , 2007, Plant Physiology.

[10]  T. Yamaya,et al.  Assimilation of ammonium ions and reutilization of nitrogen in rice (Oryza sativa L.). , 2007, Journal of experimental botany.

[11]  Kunpeng Li,et al.  Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants , 2007, Proteomics.

[12]  Hitoshi Sakakibara,et al.  Interactions between nitrogen and cytokinin in the regulation of metabolism and development. , 2006, Trends in plant science.

[13]  A. Nordheim,et al.  Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1 , 2006, Proteomics.

[14]  Marcella L Card,et al.  Arabidopsis thaliana beta-Glucosidases BGLU45 and BGLU46 hydrolyse monolignol glucosides. , 2006, Phytochemistry.

[15]  M. Sauer,et al.  Proteomic dissection of plant development , 2006, Proteomics.

[16]  Hitoshi Sakakibara,et al.  Cytokinins: activity, biosynthesis, and translocation. , 2006, Annual review of plant biology.

[17]  A. Nordheim,et al.  Proteomic analysis of shoot‐borne root initiation in maize (Zea mays L.) , 2006, Proteomics.

[18]  R. E. Sharp,et al.  Cell Wall Proteome in the Maize Primary Root Elongation Zone. I. Extraction and Identification of Water-Soluble and Lightly Ionically Bound Proteins1 , 2005, Plant Physiology.

[19]  P. Schnable,et al.  The accumulation of abundant soluble proteins changes early in the development of the primary roots of maize (Zea mays L.) , 2005, Proteomics.

[20]  C. Tatout,et al.  UDP-glucose dehydrogenases of maize: a role in cell wall pentose biosynthesis. , 2005, The Biochemical journal.

[21]  P. Schnable,et al.  Isolation, Characterization, and Pericycle-Specific Transcriptome Analyses of the Novel Maize Lateral and Seminal Root Initiation Mutant rum11[w] , 2005, Plant Physiology.

[22]  P. Schnable,et al.  The roothairless1 Gene of Maize Encodes a Homolog of sec3, Which Is Involved in Polar Exocytosis1 , 2005, Plant Physiology.

[23]  Tal Nawy,et al.  Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞ , 2005, The Plant Cell Online.

[24]  S. J. Ambrose,et al.  The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. , 2005, The Plant journal : for cell and molecular biology.

[25]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[26]  P. Schnable,et al.  Lateral roots affect the proteome of the primary root of maize (Zea mays L.) , 2004, Plant Molecular Biology.

[27]  Markus Langhans,et al.  Role of cytokinin in the regulation of root gravitropism , 2004, Planta.

[28]  W. Park,et al.  Release of the benzoxazinoids defense molecules during lateral- and crown root emergence in Zea mays. , 2004, Journal of plant physiology.

[29]  Anders Nordström,et al.  Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. Schnable,et al.  Global expression profiling applied to plant development. , 2004, Current opinion in plant biology.

[31]  D. Shasha,et al.  A Gene Expression Map of the Arabidopsis Root , 2003, Science.

[32]  R. Quatrano,et al.  Conserved Subgroups and Developmental Regulation in the Monocot rop Gene Family1[w] , 2003, Plant Physiology.

[33]  Valérie Laucou,et al.  Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014928 , 2003, The Plant Cell Online.

[34]  S. J. Ambrose,et al.  A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. , 2003, The Plant journal : for cell and molecular biology.

[35]  R. Vaňková,et al.  O-Glucosylation of cis-Zeatin in Maize. Characterization of Genes, Enzymes, and Endogenous Cytokinins1 , 2003, Plant Physiology.

[36]  J. Friml,et al.  Auxin transport - shaping the plant. , 2003, Current opinion in plant biology.

[37]  Hitoshi Sakakibara,et al.  Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. , 2002, Journal of experimental botany.

[38]  F. Lottspeich,et al.  Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize. , 2002, The Plant journal : for cell and molecular biology.

[39]  D. Blanchard,et al.  Identification of β-Glucosidase Aggregating Factor (BGAF) and Mapping of BGAF Binding Regions on Maize β-Glucosidase* , 2001, The Journal of Biological Chemistry.

[40]  A L Burlingame,et al.  Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. , 2000, Plant physiology.

[41]  D. N. Perkins,et al.  Probability‐based protein identification by searching sequence databases using mass spectrometry data , 1999, Electrophoresis.

[42]  A. Esen,et al.  Expression of soluble and catalytically active plant (monocot) beta-glucosidases in E. coli. , 1999, Biotechnology and bioengineering.

[43]  Jackson,et al.  Source and magnitude of ammonium generation in maize roots , 1998, Plant physiology.

[44]  P. Chourey,et al.  Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis , 1998, Molecular and General Genetics MGG.

[45]  G. Coruzzi,et al.  THE MOLECULAR-GENETICS OF NITROGEN ASSIMILATION INTO AMINO ACIDS IN HIGHER PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[46]  M. Evans,et al.  Specialized Zones of Development in Roots , 1995, Plant physiology.

[47]  K. Palme,et al.  Release of active cytokinin by a beta-glucosidase localized to the maize root meristem. , 1993, Science.

[48]  H. Niemeyer,et al.  Partial purification and characterization of a hydroxamic acid glucoside β-d-glucosidase from maize , 1992 .

[49]  K. Koch,et al.  Sugar Levels Modulate Differential Expression of Maize Sucrose Synthase Genes. , 1992, The Plant cell.

[50]  Alan Agresti,et al.  Categorical Data Analysis , 2003 .

[51]  H. Marschner.  Mineral Nutrition of Higher Plants , 1988 .

[52]  E. Weiler,et al.  Monoclonal Antibodies to Plant Growth Regulators: III. Zeatinriboside and Dihydrozeatinriboside. , 1986, Plant physiology.

[53]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[54]  M. Mccully,et al.  Polychromatic staining of plant cell walls by toluidine blue O , 1964, Protoplasma.

[55]  Frank Hochholdinger,et al.  The Maize Root System: Morphology, Anatomy, and Genetics , 2009 .

[56]  Journal of Experimental Botany Advance Access published May 31, 2008 Journal of Experimental Botany, Page 1 of 14 , 2008 .

[57]  P. Schnable,et al.  Isolation, Characterization, and Pericycle-Specific Transcriptome Analyses of the Novel Maize Lateral and Seminal Root Initiation Mutant rum1 1[w] , 2005 .

[58]  Woong June Park,et al.  From weeds to crops: genetic analysis of root development in cereals. , 2004, Trends in plant science.

[59]  P. Chourey,et al.  Sucrose synthase isozyme SUS1 in the maize root cap is preferentially localized in the endopolyploid outer cells , 2004 .

[60]  Wilhelm Gruissem,et al.  Biochemistry & Molecular Biology of Plants , 2002 .

[61]  D. Blanchard,et al.  Identification of beta-glucosidase aggregating factor (BGAF) and mapping of BGAF binding regions on Maize beta -glucosidase. , 2001, The Journal of biological chemistry.

[62]  P. Raymond,et al.  Metabolic regulation of asparagine synthetase gene expression in maize (Zea mays L.) root tips. , 1996, The Plant journal : for cell and molecular biology.

[63]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[64]  V. Neuhoff,et al.  Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G‐250 and R‐250 , 1988, Electrophoresis.

[65]  K. Joy,et al.  The metabolism of asparagine in plants , 1988 .

[66]  M. Zivy,et al.  Technical improvements in two‐dimensional electrophoresis increase the level of genetic variation detected in wheat‐seedling proteins , 1986 .

[67]  C. Givan.  Metabolic detoxification of ammonia in tissues of higher plants , 1979 .

[68]  E. Neufeld,et al.  CARBOHYDRATE METABOLISM. , 1965, Annual review of biochemistry.