Metabolic pathways of the wheat (Triticum aestivum) endosperm amyloplast revealed by proteomics

BackgroundBy definition, amyloplasts are plastids specialized for starch production. However, a proteomic study of amyloplasts isolated from wheat (Triticum aestivum Butte 86) endosperm at 10 days after anthesis (DPA) detected enzymes from many other metabolic and biosynthetic pathways. To better understand the role of amyloplasts in food production, the data from that study were evaluated in detail and an amyloplast metabolic map was outlined.ResultsAnalysis of 288 proteins detected in an amyloplast preparation predicted that 178 were amyloplast proteins. Criteria included homology with known plastid proteins, prediction of a plastid transit peptide for the wheat gene product or a close homolog, known plastid location of the pathway, and predicted plastid location for other members of the same pathway. Of these, 135 enzymes were arranged into 18 pathways for carbohydrate, lipid, amino acid, nucleic acid and other biosynthetic processes that are critical for grain-fill. Functions of the other proteins are also discussed.ConclusionThe pathways outlined in this paper suggest that amyloplasts play a central role in endosperm metabolism. The interacting effects of genetics and environment on starch and protein production may be mediated in part by regulatory mechanisms within this organelle.

[1]  A. Keys,et al.  The Role of the Scutellum of Cereal Seedlings in the Synthesis and Transport of Sucrose , 1959 .

[2]  B. Pogson,et al.  Vitamin synthesis in plants: tocopherols and carotenoids. , 2006, Annual review of plant biology.

[3]  S. Altenbach,et al.  Omega gliadin genes expressed in Triticum aestivum cv. Butte 86: Effects of post-anthesis fertilizer on transcript accumulation during grain development , 2007 .

[4]  B. Aral,et al.  The proline biosynthesis in living organisms , 1997, Amino Acids.

[5]  J. Prioul,et al.  Developmental Analysis of Maize Endosperm Proteome Suggests a Pivotal Role for Pyruvate Orthophosphate Dikinase1[W][OA] , 2007, Plant Physiology.

[6]  K. Palczewski,et al.  Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. , 2005, Trends in plant science.

[7]  J. Biebel SOME EFFECTS OF RADIANT ENERGY IN RELATION TO ETIOLATION. , 1942, Plant physiology.

[8]  Bo Shen,et al.  The role of 5′-adenylylsulfate reductase in controlling sulfate reduction in plants , 2005, Photosynthesis Research.

[9]  N. Kruger,et al.  The oxidative pentose phosphate pathway: structure and organisation. , 2003, Current opinion in plant biology.

[10]  S. Storozhenko,et al.  Folates in plants: biosynthesis, distribution, and enhancement , 2006 .

[11]  T. P. O’brien,et al.  The development of the wheat embryo in relation to the neighbouring tissues , 1983, Protoplasma.

[12]  K. Fischer,et al.  Analysis of the Plastidic phosphate translocator Gene Family in Arabidopsis and Identification of New phosphate translocator-Homologous Transporters, Classified by Their Putative Substrate-Binding Site1 , 2003, Plant Physiology.

[13]  R. Azevedo,et al.  The aspartic acid metabolic pathway, an exciting and essential pathway in plants , 2006, Amino Acids.

[14]  C. Jenner,et al.  Substrate gradients and regional patterns of dry matter deposition within developing wheat endosperm. I. Carbohydrates. , 1990 .

[15]  D. Bechtel,et al.  Effect of temperature on expression of genes encoding enzymes for starch biosynthesis in developing wheat endosperm , 2003 .

[16]  M. Fitzgerald,et al.  Physiological and metabolic origin of sulphur for the synthesis of seed storage proteins , 2001 .

[17]  A. Bacher,et al.  Folate synthesis in plants: The first step of the pterin branch is mediated by a unique bimodular GTP cyclohydrolase I , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Okubara,et al.  Symbiotic root nodules of the actinorhizal plant Datisca glomerata express Rubisco activase mRNA. , 1999, Plant physiology.

[19]  J. Lunn Compartmentation in plant metabolism. , 2006, Journal of experimental botany.

[20]  A. Subramanian,et al.  The Plastid Ribosomal Proteins , 2000, The Journal of Biological Chemistry.

[21]  J. Schwender,et al.  Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds , 2004, Nature.

[22]  K. Edwards,et al.  Two Cytosolic Glutamine Synthetase Isoforms of Maize Are Specifically Involved in the Control of Grain Production[W][OA] , 2006, The Plant Cell Online.

[23]  T. ap Rees,et al.  Starch synthesis by isolated amyloplasts from wheat endosperm , 1988, Planta.

[24]  J. Porter,et al.  Modelling protein content and composition in relation to crop nitrogen dynamics for wheat , 2006 .

[25]  M. Akita,et al.  Early Steps in the Biosynthesis of NAD in Arabidopsis Start with Aspartate and Occur in the Plastid1 , 2006, Plant Physiology.

[26]  C. Atkins,et al.  Reexamination of the Intracellular Localization of de Novo Purine Synthesis in Cowpea Nodules , 1997, Plant physiology.

[27]  A. Weber,et al.  Spinach hexokinase I is located in the outer envelope membrane of plastids , 1999, FEBS letters.

[28]  C. Bhatia,et al.  Bioenergetic Considerations in Cereal Breeding for Protein Improvement , 1976, Science.

[29]  S. Altenbach,et al.  Expression of 9-kDa non-specific lipid transfer protein genes in developing wheat grain is enhanced by high temperatures but not by post-anthesis fertilizer , 2008 .

[30]  M. Burrell,et al.  Starch synthesis and carbon partitioning in developing endosperm. , 2003, Journal of experimental botany.

[31]  F. Dupont,et al.  Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. , 2006, Journal of experimental botany.

[32]  R. Allen,et al.  Dissection of Oxidative Stress Tolerance Using Transgenic Plants , 1995, Plant physiology.

[33]  Daniel B. Martin,et al.  Computational prediction of proteotypic peptides for quantitative proteomics , 2007, Nature Biotechnology.

[34]  T. Leustek,et al.  Evidence for the thiamine biosynthetic pathway in higher-plant plastids and its developmental regulation , 1995, Plant Molecular Biology.

[35]  D. Randall,et al.  Regulation of pyruvate dehydrogenase complex activity in plant cells. , 2003, European journal of biochemistry.

[36]  C. Jenner,et al.  High Temperature Affects the Activity of Enzymes in the Committed Pathway of Starch Synthesis in Developing Wheat Endosperm , 1993 .

[37]  W Zerges,et al.  Translation in chloroplasts. , 2000, Biochimie.

[38]  W. Sakamoto Protein degradation machineries in plastids. , 2006, Annual review of plant biology.

[39]  Atilio J Barneix,et al.  Physiology and biochemistry of source-regulated protein accumulation in the wheat grain. , 2007, Journal of plant physiology.

[40]  C. Jenner,et al.  Substrate gradients and regional patterns of dry matter deposition within developing wheat endosperm. II, Amino acids and protein , 1990 .

[41]  A. Hanson,et al.  ONE-CARBON METABOLISM IN HIGHER PLANTS. , 2001, Annual review of plant physiology and plant molecular biology.

[42]  Anthony Maxwell,et al.  Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. B. Fisher,et al.  Accumulation and Conversion of Sugars by Developing Wheat Grains : VI. Gradients Along the Transport Pathway from the Peduncle to the Endosperm Cavity during Grain Filling. , 1986, Plant physiology.

[44]  N. Stuurman,et al.  B-type granule containing protrusions and interconnections between amyloplasts in developing wheat endosperm revealed by transmission electron microscopy and GFP expression. , 2000, Journal of experimental botany.

[45]  Robert P. Wilson,et al.  Amino acids and proteins , 2003 .

[46]  B. Feil,et al.  Competition between Nitrogen Accumulation and Grain Growth for Carbohydrates during Grain Filling of Wheat , 1994 .

[47]  G. Gloor,et al.  The Hsp90 family of proteins in Arabidopsis thaliana , 2001, Cell stress & chaperones.

[48]  W. Plaxton,et al.  THE ORGANIZATION AND REGULATION OF PLANT GLYCOLYSIS. , 1996, Annual review of plant physiology and plant molecular biology.

[49]  Ron D. Appel,et al.  ExPASy: the proteomics server for in-depth protein knowledge and analysis , 2003, Nucleic Acids Res..

[50]  T. ap Rees,et al.  Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. , 1990, The Biochemical journal.

[51]  T. Takao,et al.  Multiple iso‐proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation , 2005 .

[52]  M. Tamoi,et al.  Regulation and function of ascorbate peroxidase isoenzymes. , 2002, Journal of experimental botany.

[53]  M. Wirtz,et al.  Synthesis of the sulfur amino acids: cysteine and methionine , 2005, Photosynthesis Research.

[54]  D. Aspinall,et al.  The physiology of starch and protein deposition in the endosperm of wheat. , 1990 .

[55]  Y. Meyer,et al.  Resemblance and Dissemblance of Arabidopsis Type II Peroxiredoxins: Similar Sequences for Divergent Gene Expression, Protein Localization, and Activity1 , 2003, Plant Physiology.

[56]  J. Froehlich,et al.  A Stromal Hsp100 Protein Is Required for Normal Chloroplast Development and Function in Arabidopsis1[w] , 2004, Plant Physiology.

[57]  What Are All Those Funny Symbols in a Blast Printout? Blast = Basic Local Alignment Search Tool , 2022 .

[58]  A. Bacher,et al.  Biosynthesis of vitamin b2 (riboflavin). , 2000, Annual review of nutrition.

[59]  John R Yates,et al.  Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry , 2002, Proteomics.

[60]  M. F. Drincovich,et al.  NADP‐malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways , 2001, FEBS letters.

[61]  D. B. Fisher,et al.  Amino Acid Composition Along the Transport Pathway during Grain Filling in Wheat. , 1986, Plant physiology.

[62]  P. M. Baldwin Starch granule-associated proteins and polypeptides : A review , 2001 .

[63]  S. Brunak,et al.  Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. , 2000, Journal of molecular biology.

[64]  B. Brown,et al.  Irrigated hard winter wheat response to fall, spring, and late season applied nitrogen , 2006 .

[65]  K. V. van Wijk Plastid proteomics. , 2004, Plant physiology and biochemistry : PPB.

[66]  Cassie Aldridge,et al.  The molecular biology of plastid division in higher plants. , 2005, Journal of experimental botany.

[67]  S. Kopriva Regulation of sulfate assimilation in Arabidopsis and beyond. , 2006, Annals of botany.

[68]  Ronald Chan,et al.  Temperature, Water and Fertilizer Influence the Timing of Key Events During Grain Development in a US Spring Wheat , 2003 .

[69]  Nick Cai,et al.  A complete ferredoxin/thioredoxin system regulates fundamental processes in amyloplasts. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[70]  D. B. Fowler,et al.  Crop Nitrogen Demand and Grain Protein Concentration of Spring and Winter Wheat , 2003 .

[71]  D. Huggins,et al.  Economically Optimal Nitrogen Fertilization for Yield and Protein in Hard Red Spring Wheat , 2004, Agronomy Journal.

[72]  B. Grimm,et al.  Cytokinin effects on tetrapyrrole biosynthesis and photosynthetic activity in barley seedlings , 2006, Planta.

[73]  P. Keeling,et al.  The Major Form of ADP-Glucose Pyrophosphorylase in Maize Endosperm Is Extra-Plastidial , 1996, Plant physiology.

[74]  D. Bechtel,et al.  Amyloplast Formation and Starch Granule Development in Hard Red Winter Wheat , 2003 .

[75]  A. Subramanian,et al.  The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). , 2000, The Journal of biological chemistry.

[76]  E. López-Juez Plastid biogenesis, between light and shadows. , 2006, Journal of experimental botany.

[77]  N. Simmonds,et al.  The relation between yield and protein in cereal grain , 1995 .

[78]  D. Wettstein,et al.  tRNAGlu as a cofactor in δ-aminolevulinate biosynthesis: steps that regulate chlorophyll synthesis , 1988 .

[79]  S. Elhani,et al.  Protein and lysine content, grain yield, and other technological traits in durum wheat under Mediterranean conditions. , 2001, Journal of agricultural and food chemistry.

[80]  K. Saito,et al.  Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana , 2001, Amino Acids.

[81]  W. Vensel,et al.  Developmental changes in the metabolic protein profiles of wheat endosperm , 2005, Proteomics.

[82]  F. Oury,et al.  Yield and grain protein concentration in bread wheat: how to use the negative relationship between the two characters to identify favourable genotypes? , 2007, Euphytica.

[83]  H. Ashihara,et al.  Purine and pyrimidine nucleotide metabolism in higher plants. , 2003, Journal of plant physiology.

[84]  Antje Chang,et al.  BRENDA , the enzyme database : updates and major new developments , 2003 .

[85]  F. Dupont,et al.  Differential accumulation of sulfur-rich and sulfur-poor wheat flour proteins is affected by temperature and mineral nutrition during grain development , 2006 .

[86]  I. Tetlow,et al.  Characterization of ADP-glucose transport across the cereal endosperm amyloplast envelope. , 2007, Journal of experimental botany.

[87]  S. Richter,et al.  Function of the stromal processing peptidase in the chloroplast import pathway , 2005 .

[88]  J. Schmid,et al.  Molecular organization of the shikimate pathway in higher plants , 1995 .

[89]  A. Fürholz,et al.  Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[90]  M. Emes,et al.  NONPHOTOSYNTHETIC METABOLISM IN PLASTIDS. , 2003, Annual review of plant physiology and plant molecular biology.

[91]  Jaroslaw Pillardy,et al.  Clp Protease Complexes from Photosynthetic and Non-photosynthetic Plastids and Mitochondria of Plants, Their Predicted Three-dimensional Structures, and Functional Implications* , 2004, Journal of Biological Chemistry.

[92]  J. Soll,et al.  From nuclear genes to chloroplast localized proteins , 2001 .

[93]  K. Sjölander,et al.  The Arabidopsis thaliana Chloroplast Proteome Reveals Pathway Abundance and Novel Protein Functions , 2004, Current Biology.

[94]  M. J. Pimenta,et al.  S-Methylmethionine Plays a Major Role in Phloem Sulfur Transport and Is Synthesized by a Novel Type of Methyltransferase , 1999, Plant Cell.