Metabolomic and proteomic changes in the xylem sap of maize under drought.

Plants produce compounds in roots that are transported to shoots via the xylem sap. Some of these compounds are vital for signalling and adaptation to environmental stress such as drought. In this study, we screened the xylem sap using mass spectrometry to quantify the changes in new and previously identified sap constituents under extended drought. We detected and quantified the changes in the concentration of 31 compounds present in the xylem sap under progressively increasing drought stress. We found changes in the hormones abscisic acid (ABA) and cytokinin, and the presence of high concentrations of the aromatic cytokinin 6-benzylaminopurine (BAP). Several phenylpropanoid compounds (coumaric, caffeic and ferulic acids) were found in xylem sap. The concentrations of some of these phenylpropanoid compounds changed under drought. In parallel, an analysis of the xylem sap proteome was conducted. We found a higher abundance of cationic peroxidases, which with the increase in phenylpropanoids may lead to a reduction in lignin biosynthesis in the xylem vessels and could induce cell wall stiffening. The application of new methodologies provides insights into the range of compounds in sap and how alterations in composition may lead to changes in development and signalling during adaptation to drought.

[1]  R. E. Sharp,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.

[2]  G. Pearce,et al.  Systemin: a polypeptide signal for plant defensive genes. , 1998, Annual review of cell and developmental biology.

[3]  H. Wolterbeek,et al.  Analysis of major tomato xylem organic acids and PITC-derivatives of amino acids by RP-HPLC and UV detection , 1992, Plant and Soil.

[4]  Jørgen Holst Christensen,et al.  Purification and characterization of peroxidases correlated with lignification in poplar xylem. , 1998, Plant physiology.

[5]  A. Bano,et al.  Changes in the contents of free and conjugated abscisic acid, phaseic acid and cytokinins in xylem sap of drought stressed sunflower plants , 1994 .

[6]  G. Boyer,et al.  Accumulation and transport of abscisic Acid and its metabolites in ricinus and xanthium. , 1984, Plant physiology.

[7]  Jianhua Zhang,et al.  Comparison of exportation and metabolism of xylem-delivered ABA in maize leaves at different water status and xylem sap pH , 2004, Plant Growth Regulation.

[8]  J. Kehr,et al.  Xylem sap protein composition is conserved among different plant species , 2004, Planta.

[9]  Jing Liu,et al.  Dynamic analysis of ABA accumulation in relation to the rate of ABA catabolism in maize tissues under water deficit. , 2006, Journal of experimental botany.

[10]  N. Holbrook,et al.  Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. , 2002, Journal of experimental botany.

[11]  Chung-Jui Tsai,et al.  Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees , 1999, Nature Biotechnology.

[12]  W. Hartung,et al.  Extracellular beta-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. , 2000, Journal of experimental botany.

[13]  C. Dunand,et al.  Performing the paradoxical: how plant peroxidases modify the cell wall. , 2004, Trends in plant science.

[14]  M. Sugiyama,et al.  Separation and characterization of the isoenzymes of wall-bound peroxidase from cultured Zinnia cells during tracheary element differentiation , 1995, Planta.

[15]  C. D. de Koster,et al.  A tomato xylem sap protein represents a new family of small cysteine‐rich proteins with structural similarity to lipid transfer proteins , 2003, FEBS letters.

[16]  B. Sundberg,et al.  Xyloglucan Endotransglycosylases Have a Function during the Formation of Secondary Cell Walls of Vascular Tissues Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007773. , 2002, The Plant Cell Online.

[17]  I. Dodd Hormonal Interactions and Stomatal Responses , 2003, Journal of Plant Growth Regulation.

[18]  W. Hartung,et al.  A possible stress physiological role of abscisic acid conjugates in root-to-shoot signalling. , 2002, Plant, cell & environment.

[19]  E. Schulze,et al.  The concentration of xylem sap constituents in root exudate, and in sap from intact, transpiring castor bean plants (Ricinus communis L.) , 1995 .

[20]  T. Sharkey,et al.  Effects of phaseic Acid and dihydrophaseic Acid on stomata and the photosynthetic apparatus. , 1980, Plant physiology.

[21]  R. E. Sharp,et al.  Proline Accumulation in Maize (Zea mays L.) Primary Roots at Low Water Potentials (I. Requirement for Increased Levels of Abscisic Acid) , 1994, Plant physiology.

[22]  W. Hartung,et al.  Radial transport of abscisic acid conjugates in maize roots: its implication for long distance stress signals. , 2000, Journal of experimental botany.

[23]  H. Fukui,et al.  A novel abscisic acid metabolite from seeds of Robinia pseudacacia , 1978 .

[24]  Y. Matsubayashi,et al.  Peptide hormones in plants. , 2006, Annual review of plant biology.

[25]  J. Pate,et al.  Transport, synthesis and catabolism of abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L.) under phosphate deficiency and moderate salinity , 1997 .

[26]  Ulrich Schurr,et al.  Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus. II.Stomatal sensitivity to abscisic acid imported from the xylem sap , 1992 .

[27]  G. Pearce,et al.  RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Fan Jiang,et al.  Activation of Glucosidase via Stress-Induced Polymerization Rapidly Increases Active Pools of Abscisic Acid , 2006, Cell.

[29]  D. Davies,et al.  The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. , 2002, Journal of experimental botany.

[30]  I. Rayment,et al.  Structure and Function of Enzymes of the Leloir Pathway for Galactose Metabolism* , 2003, Journal of Biological Chemistry.

[31]  H. Matsui,et al.  A large family of class III plant peroxidases. , 2001, Plant & cell physiology.

[32]  R. E. Sharp,et al.  Relationships between xylem sap constituents and leaf conductance of well-watered and water-stressed maize across three xylem sap sampling techniques. , 2005, Journal of experimental botany.

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

[34]  A. Altman,et al.  Presence and identification of polyamines in xylem and Phloem exudates of plants. , 1986, Plant physiology.

[35]  H. Bohnert,et al.  Convergent Induction of Osmotic Stress-Responses : Abscisic Acid, Cytokinin, and the Effects of NaCl. , 1992, Plant physiology.

[36]  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.

[37]  Johann Joets,et al.  PROTICdb: A web‐based application to store, track, query, and compare plant proteome data , 2005, Proteomics.

[38]  J. Pospíšilová,et al.  Effects of Pre-Treatments with Abscisic Acid and/or Benzyladenine on Gas Exchange of French Bean, Sugar Beet, and Maize Leaves During Water Stress and After Rehydration , 2004, Biologia Plantarum.

[39]  W. Hartung,et al.  The uptake and flow of C, N and ions between roots and shoots in Ricinus communis L. III. Long-distance transport of abscisic acid depending on nitrogen nutrition and salt stress , 1994 .

[40]  Sixue Chen,et al.  Characterization of the maize xylem sap proteome. , 2006, Journal of proteome research.

[41]  C. Lapierre,et al.  Water Deficits Affect Caffeate O-Methyltransferase, Lignification, and Related Enzymes in Maize Leaves. A Proteomic Investigation1[w] , 2005, Plant Physiology.

[42]  R. Munns,et al.  Abscisic Acid is not the only stomatal inhibitor in the transpiration stream of wheat plants. , 1988, Plant physiology.

[43]  J. Deikman,et al.  Induction of Anthocyanin Accumulation by Cytokinins in Arabidopsis thaliana , 1995, Plant physiology.

[44]  Z. Minić,et al.  Cell Wall Proteome , 2007 .

[45]  G. Pearce,et al.  Systemic Signaling in Tomato Plants for Defense against Herbivores , 2003, Journal of Biological Chemistry.

[46]  W Hartung,et al.  The long-distance abscisic acid signal in the droughted plant: the fate of the hormone on its way from root to shoot. , 2001, Journal of experimental botany.

[47]  M. Strnad The aromatic cytokinins , 1997 .

[48]  W. J. Davies,et al.  ABA-based chemical signalling: the co-ordination of responses to stress in plants. , 2002, Plant, cell & environment.

[49]  J. Ralph,et al.  Combinatorial modification of multiple lignin traits in trees through multigene cotransformation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  G. Sagar,et al.  THE EFFECT OF ROOT PRUNING AND 6-BENZYL-AMINOPURINE ON THE CHLOROPHYLL CONTENT, 14CO2 FIXATION AND THE SHOOT/ROOT RATIO IN SEEDLINGS OF PISVM SATIVUM L. , 1973 .

[51]  J. Leach,et al.  Rice Cationic Peroxidase Accumulates in Xylem Vessels during Incompatible Interactions with Xanthomonas oryzae pv oryzae , 1995, Plant physiology.

[52]  C. D. de Koster,et al.  Mass Spectrometric Identification of Isoforms of PR Proteins in Xylem Sap of Fungus-Infected Tomato1 , 2002, Plant Physiology.

[53]  C. Gehring,et al.  Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues , 2001 .

[54]  Julian I. Schroeder,et al.  Guard cell abscisic acid signalling and engineering drought hardiness in plants , 2001, Nature.

[55]  T. G. Prasad,et al.  Hormone Signals from Roots to Shoots of Sunflower (Helianthus annuus L.). Moderate Soil Drying Increases Delivery of Abscisic Acid and Depresses Delivery of Cytokinins in Xylem Sap , 1996 .

[56]  Ulrich Schurr,et al.  Stomatal response to drying soil in relation to changes in the xylem sap composition of Helianthus annuus. I. The concentration of cations, anions, amino acids in, and pH of, the xylem sap , 1992 .

[57]  J. Pospíšilová Participation of Phytohormones in the Stomatal Regulation of Gas Exchange During Water Stress , 2003, Biologia Plantarum.

[58]  F. B. Abeles,et al.  Xylem sap proteins. , 1991, Plant physiology.

[59]  N. C. Veitch,et al.  Horseradish peroxidase: a modern view of a classic enzyme. , 2004, Phytochemistry.

[60]  S. Kawai,et al.  Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics , 2003, Journal of Plant Research.

[61]  W. Davies,et al.  Long-distance ABA Signaling and Its Relation to Other Signaling Pathways in the Detection of Soil Drying and the Mediation of the Plant’s Response to Drought , 2005, Journal of Plant Growth Regulation.

[62]  J. Peltier,et al.  Drought-induced increase in xylem malate and mannitol concentrations and closure of Fraxinus excelsior L. stomata , 1999 .

[63]  F. Asch,et al.  Drought-induced changes in xylem pH, ionic composition, and ABA concentration act as early signals in field-grown maize (Zea mays L.). , 2002, Journal of experimental botany.

[64]  D J Cosgrove,et al.  Enzymes and other agents that enhance cell wall extensibility. , 1999, Annual review of plant physiology and plant molecular biology.

[65]  P. Giavalisco,et al.  Analysis of xylem sap proteins from Brassica napus , 2005, BMC Plant Biology.