skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis

Journal Article · · Journal of Experimental Botany
DOI:https://doi.org/10.1093/jxb/ern198· OSTI ID:1625356
 [1];  [1];  [2];  [2];  [1]
  1. Institut National de la Recherche Agronomique, Nantes Cedex (France). Unite de Recherche Biopolymeres, Interactions, Assemblages
  2. Iowa State Univ., Ames, IA (United States). Dept. of Biochemistry, Biophysics and Molecular Biology

In addition to the exclusively granule-bound starch synthase GBSSI, starch granules also bind significant proportions of other starch biosynthetic enzymes, particularly starch synthases (SS) SSI and SSIIa, and starch branching enzyme (BE) BEIIb. Whether this association is a functional aspect of starch biosynthesis, or results from non-specific entrapment during amylopectin crystallization, is not known. This study utilized genetic, immunological, and proteomic approaches to investigate comprehensively the proteome and phosphoproteome of Zea mays endosperm starch granules. SSIII, BEI, BEIIa, and starch phosphorylase were identified as internal granule-associated proteins in maize endosperm, along with the previously identified proteins GBSS, SSI, SSIIa, and BEIIb. Genetic analyses revealed three instances in which granule association of one protein is affected by the absence of another biosynthetic enzyme. First, eliminating SSIIa caused reduced granule association of SSI and BEIIb, without affecting GBSS abundance. Second, eliminating SSIII caused the appearance of two distinct electrophoretic mobility forms of BEIIb, whereas only a single migration form of BEIIb was observed in wild type or any other mutant granules examined. Third, eliminating BEIIb caused significant increases in the abundance of BEI, BEIIa, SSIII, and starch phosphorylase in the granule, without affecting SSI or SSIIa. Analysis of the granule phosphoproteome with a phosphorylation-specific dye indicated that GBSS, BEIIb, and starch phosphorylase are all phosphorylated as they occur in the granule. These results suggest the possibility that starch metabolic enzymes located in granules are regulated by posttranslational modification and/or protein–protein interactions

Research Organization:
Iowa State Univ., Ames, IA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
FG02-05ER15706
OSTI ID:
1625356
Journal Information:
Journal of Experimental Botany, Vol. 59, Issue 12; ISSN 0022-0957
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (55)

Recent Progress toward Understanding Biosynthesis of the Amylopectin Crystal journal April 2000
Biochemical and molecular characterization of a novel starch synthase from potato tubers journal August 1995
Molecular analysis of the waxy locus of Zea mays journal May 1986
The Synthesis of the Starch Granule journal June 1997
Molecular identification and isolation of the Waxy locus in maize journal November 1983
Isolation and characterization of the zSSIIa and zSSIIb starch synthase cDNA clones from maize endosperm journal January 1998
Differentiation of the Properties of the Branching Isozymes from Maize (Zea mays) journal August 1993
Compartmentation of the Starch-Related R1 Protein in Higher Plants journal June 2000
Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa journal April 2004
Association of a 76 kDa polypeptide with soluble starch synthase I activity in maize (cv B73) endosperm journal August 1994
Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels journal January 1987
Independent Genetic Control of Maize Starch-Branching Enzymes IIa and IIb (Isolation and Characterization of a Sbe2a cDNA) journal May 1997
Evidence for the Inclusion of Controlling Elements Within the Structural gene at the waxy Locus in Maize journal October 1981
Characterization of dull1 , a Maize Gene Coding for a Novel Starch Synthase journal March 1998
Global quantitative phosphoprotein analysis using Multiplexed Proteomics technology journal July 2003
Protein Phosphorylation in Amyloplasts Regulates Starch Branching Enzyme Activity and Protein–Protein Interactions journal February 2004
Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties journal April 2003
The Relation of Starch Phosphorylases to Starch Metabolism in Wheat journal October 2004
Allelic Analysis of the Maize amylose-extender Locus Suggests That Independent Genes Encode Starch-Branching Enzymes IIa and IIb journal February 1996
Purification and Characterization of the Maize Amyloplast Stromal 112-kDa Starch Phosphorylase journal April 2001
Starch Biosynthetic Enzymes from Developing Maize Endosperm Associate in Multisubunit Complexes journal February 2008
Genetic Isolation, Cloning, and Analysis of a Mutator-Induced, Dominant Antimorph of the Maize amylose extender1 Locus. journal November 1993
Plastidial α -Glucan Phosphorylase Is Not Required for Starch Degradation in Arabidopsis Leaves But Has a Role in the Tolerance of Abiotic Stress journal June 2004
Identification of Mutator Insertional Mutants of Starch-Branching Enzyme 2a in Corn journal March 2001
Function and Characterization of Starch Synthase I Using Mutants in Rice journal January 2006
Current two-dimensional electrophoresis technology for proteomics journal November 2004
The elongation of amylose and amylopectin chains in isolated starch granules journal December 1996
The function of the Waxy locus in starch synthesis in maize endosperm journal February 1974
The barley starch granule proteome—internalized granule polypeptides of the mature endosperm journal March 2004
Genetic Isolation, Cloning, and Analysis of a Mutator-Induced, Dominant Antimorph of the Maize amylose extender1 Locus journal November 1993
Sequence conservation of the catalytic regions of anylolytic enzymes in maize branching enzyme-I journal November 1991
Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii journal October 2006
Identification of the Soluble Starch Synthase Activities of Maize Endosperm journal May 1999
Starch branching enzyme IIb in wheat is expressed at low levels in the endosperm compared to other cereals and encoded at a non-syntenic locus journal September 2005
Starch-Branching Enzymes Preferentially Associated with A-Type Starch Granules in Wheat Endosperm journal September 2000
Physical Association of Starch Biosynthetic Enzymes with Starch Granules of Maize Endosperm (Granule-Associated Forms of Starch Synthase I and Starch Branching Enzyme II) journal July 1996
The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation: Function of starch synthase type IV journal January 2007
Single-nucleotide polymorphisms in rice starch synthase IIa that alter starch gelatinisation and starch association of the enzyme journal January 2005
Cloning and characterization of a gene encoding wheat starch synthase I journal June 1999
Evidence for Independent Genetic Control of the Multiple Forms of Maize Endosperm Branching Enzymes and Starch Synthases journal June 1981
F ROM B ACTERIAL G LYCOGEN TO S TARCH : Understanding the Biogenesis of the Plant Starch Granule journal June 2003
Starch Branching Enzyme II from Maize Endosperm journal July 1993
Multiple forms of (1 → 4)-α-d-glucan, (1 → 4)-α-d-glucan-6- glycosyl transferase from developing zea mays L. Kernels journal March 1978
Recent developments in understanding the regulation of starch metabolism in higher plants journal September 2004
A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis journal February 1995
Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos journal July 1993
The Major Proteins of Wheat Endosperm Starch Granules journal January 1995
Analysis of Protein Complexes in Wheat Amyloplasts Reveals Functional Interactions among Starch Biosynthetic Enzymes journal February 2008
Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose journal July 2000
Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. journal January 2002
Compartmentation of the Starch-Related R1 Protein in Higher Plants journal July 2000
Starch synthesis in the cereal endosperm journal June 2003
Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves: SSI mutant of Arabidopsis journal July 2005
Effects of Amylopectin Branch Chain Length and Amylose Content on the Gelatinization and Pasting Properties of Starch journal September 1999
Mutations at the Shrunken-4 Locus in Maize that Produce Three Altered Phosphorylases journal April 1969

Cited By (38)

A review of starch-branching enzymes and their role in amylopectin biosynthesis: Starch-Branching Enzymes In Amylopectin Biosynthesis journal August 2014
Deficiency of maize starch-branching enzyme i results in altered starch fine structure, decreased digestibility and reduced coleoptile growth during germination journal January 2011
Starch synthase 4 is located in the thylakoid membrane and interacts with plastoglobule-associated proteins in Arabidopsis journal September 2014
Development of high amylose wheat through TILLING journal January 2012
In vivo phosphoproteome characterization reveals key starch granule-binding phosphoproteins involved in wheat water-deficit response journal October 2017
Post-translational Modifications in Regulation of Chloroplast Function: Recent Advances journal February 2017
Self-preserving lognormal volume-size distributions of starch granules in developing sweetpotatoes and modulation of their scale parameters by a starch synthase II (SSII) journal October 2016
Protein Kinases and Phosphatases of the Plastid and Their Potential Role in Starch Metabolism journal July 2018
Cornstarch is less allergenic than corn flour in dogs and cats previously sensitized to corn journal June 2018
Proteomic Analysis of Starch Biosynthesis in Maize Seeds journal July 2019
Maize proteomics: An insight into the biology of an important cereal crop journal January 2013
Intra-Sample Heterogeneity of Potato Starch Reveals Fluctuation of Starch-Binding Proteins According to Granule Morphology journal September 2019
Quantitative phosphoproteomic analysis of early seed development in rice (Oryza sativa L.) journal November 2015
Non-GMO potato lines with an altered starch biosynthesis pathway confer increased-amylose and resistant starch properties: Non-GMO potato lines with altered starch biosynthesis journal February 2017
Recreating the synthesis of starch granules in yeast journal November 2016
Allelic effects on starch structure and properties of six starch biosynthetic genes in a rice recombinant inbred line population journal March 2015
Proteomic Dissection of Endosperm Starch Granule Associated Proteins Reveals a Network Coordinating Starch Biosynthesis and Amino Acid Metabolism and Glycolysis in Rice Endosperms journal May 2016
Starch Biosynthesis in Relation to Resistant Starch book September 2013
Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions journal November 2011
Starch Biosynthesis in Relation to Resistant Starch book September 2013
Protein-Protein Interactions During Starch Biosynthesis book January 2015
Genetic and genomic analysis of the seed-filling process in maize based on a logistic model journal July 2019
Dynamic development of starch granules and the regulation of starch biosynthesis in Brachypodium distachyon: comparison with common wheat and Aegilops peregrina journal August 2014
Increasing the amylose content of durum wheat through silencing of the SBEIIagenes journal July 2010
Formation of starch in plant cells journal May 2016
Distinct metabolic changes between wheat embryo and endosperm during grain development revealed by 2D-DIGE-based integrative proteome analysis journal April 2016
PROTEIN TARGETING TO STARCH Is Required for Localising GRANULE-BOUND STARCH SYNTHASE to Starch Granules and for Normal Amylose Synthesis in Arabidopsis text January 2015
The primitive rhodophyte Cyanidioschyzon merolae contains a semiamylopectin-type, but not an amylose-type,  -glucan journal April 2010
PROTEIN TARGETING TO STARCH Is Required for Localising GRANULE-BOUND STARCH SYNTHASE to Starch Granules and for Normal Amylose Synthesis in Arabidopsis journal February 2015
Proteome characterization of developing grains in bread wheat cultivars (Triticum aestivum L.) journal January 2012
The cereal starch endosperm development and its relationship with other endosperm tissues and embryo journal August 2014
Waxy allele diversification in foxtail millet (Setaria italica) landraces of Taiwan journal December 2018
Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation journal July 2017
iTRAQ-based quantitative proteome and phosphoprotein characterization reveals the central metabolism changes involved in wheat grain development journal January 2014
A rapid and universal method for isolating starch granules in plant tissues journal August 2019
Preferential binding of SBD from Arabidopsis thaliana SSIII to polysaccharides: Study of amino acid residues involved journal March 2011
Starch formation inside plastids of higher plants journal May 2018
Proteome Profile of Starch Granules Purified from Rice (Oryza sativa) Endosperm journal December 2016

Similar Records

Structure, function and regulation of the enzymes in the starch biosynthetic pathway.
Technical Report · Sat Nov 30 00:00:00 EST 2013 · OSTI ID:1625356

Final technical report
Technical Report · Tue Jun 08 00:00:00 EDT 2004 · OSTI ID:1625356

(Starch synthesis in the maize endosperm as affected by starch synthesizing mutants)
Technical Report · Tue Jan 01 00:00:00 EST 1985 · OSTI ID:1625356