Pyrophosphate-Dependent Fructose-6-Phosphate 1-Phosphotransferase Induction and Attenuation of Hsp Gene Expression during Endosperm Modification in Quality Protein Maize1[C][W][OA]

Quality Protein Maize (QPM) is a hard-endosperm version of the high-lysine opaque2 (o2) maize (Zea mays) mutant, but the genes involved in modification of the soft o2 endosperm are largely unknown. Pyrophosphate-dependent fructose-6-phosphate 1-phosphotransferase (PFP) catalyzes the ATP-independent conversion of fructose-6-phosphate to fructose-1,6-bisphosphate in glycolysis. We found a large increase in transcript and protein levels of the α-regulatory subunit of PFP (PFPα) in QPM endosperm. In vitro enzyme assays showed a significant increase in forward PFP activity in developing endosperm extracts of QPM relative to the wild type and o2. An expressed retrogene version of PFPα of unknown function that was not up-regulated in QPM was also identified. The elevated expression levels of a number of ATP-requiring heat shock proteins (Hsps) in o2 endosperm are ameliorated in QPM. PFPα is also coinduced with Hsps in maize roots in response to heat, cold, and the unfolded protein response stresses. We propose that reduced ATP availability resulting from the generalized Hsp response in addition to the reduction of pyruvate, orthophosphate dikinase activity in o2 endosperm is compensated in part by increased PFP activity in QPM.

[1]  Wing Hung Wong,et al.  SeqMap: mapping massive amount of oligonucleotides to the genome , 2008, Bioinform..

[2]  D. Ware,et al.  Digital Gene Expression Signatures for Maize Development1[W][OA] , 2010, Plant Physiology.

[3]  H. O. Gevers,et al.  Development of modified opaque-2 maize in South Africa , 1992 .

[4]  T. Andrews,et al.  Properties and mechanism of action of pyruvate, phosphate dikinase from leaves. , 1969, The Biochemical journal.

[5]  M. Stitt,et al.  Inorganic pyrophosphate content and metabolites in potato and tobacco plants expressing E. coli pyrophosphatase in their cytosol , 1992, Planta.

[6]  B. Larkins,et al.  Characterization of opaque2 modifier QTLs and candidate genes in recombinant inbred lines derived from the K0326Y quality protein maize inbred , 2011, Theoretical and Applied Genetics.

[7]  S. Long,et al.  Cool C4 Photosynthesis: Pyruvate Pi Dikinase Expression and Activity Corresponds to the Exceptional Cold Tolerance of Carbon Assimilation in Miscanthus × giganteus12[W][OA] , 2008, Plant Physiology.

[8]  F. Botha,et al.  Pyrophosphate Dependent Phosphofructokinase of Citrullus lanatus: Molecular Forms and Expression of Subunits. , 1991, Plant physiology.

[9]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[10]  B. Larkins,et al.  Maize Opaque Endosperm Mutations Create Extensive Changes in Patterns of Gene Expression Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003905. , 2002, The Plant Cell Online.

[11]  B. Larkins,et al.  Gamma‐Zein Content is Ralated to Endosperm Modification in Quality Protein Maize , 1991 .

[12]  M. Long,et al.  Extensive Structural Renovation of Retrogenes in the Evolution of the Populus Genome1[W][OA] , 2009, Plant Physiology.

[13]  B. Larkins,et al.  THE DEVELOPMENT AND IMPORTANCE OF ZEIN PROTEIN BODIES IN MAIZE ENDOSPERM , 2006 .

[14]  B. Larkins,et al.  Genetic analysis of opaque2 modifier gene activity in maize endosperm , 1995, Theoretical and Applied Genetics.

[15]  A. Millar,et al.  Does anoxia tolerance involve altering the energy currency towards PPi? , 2008, Trends in plant science.

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

[17]  S. Vasal,et al.  Genetic modifiers and breeding strategies in developing hard endosperm opaque-2 materials. , 1980 .

[18]  B. Larkins,et al.  RBR3, a member of the retinoblastoma-related family from maize, is regulated by the RBR1/E2F pathway. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Xuelu Wang,et al.  Altered starch structure is associated with endosperm modification in Quality Protein Maize , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  B. Larkins,et al.  New Methods for Extraction and Quantitation of Zeins Reveal a High Content of gamma-Zein in Modified opaque-2 Maize. , 1990, Plant physiology.

[21]  B. Larkins,et al.  Molecular Genetic Approaches to Maize Improvement , 2009 .

[22]  B. Larkins,et al.  The maize Mucronate mutation is a deletion in the 16-kDa gamma-zein gene that induces the unfolded protein response. , 2006, The Plant journal : for cell and molecular biology.

[23]  M. X. Wu,et al.  Pyrophosphate Fructose-6-P 1-Phosphotransferase from Tomato Fruit : Evidence for Change during Ripening. , 1990, Plant physiology.

[24]  A. Altman,et al.  Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. , 2004, Trends in plant science.

[25]  J. Messing,et al.  γ-Zeins are essential for endosperm modification in quality protein maize , 2010, Proceedings of the National Academy of Sciences of the United States of America.

[26]  B. Larkins,et al.  Genetic analysis of opaque2 modifier loci in quality protein maize , 2008, Theoretical and Applied Genetics.

[27]  J. Davies,et al.  The computed free energy change of hydrolysis of inorganic pyrophosphate and ATP: apparent significance. for inorganic-pyrophosphate-driven reactions of intermediary metabolism , 1993 .

[28]  M. S. Zuber,et al.  Lysine Content of Opaque-2 Maize Kernels having Different Phenotypes 1 , 1969 .

[29]  K. Koch,et al.  Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. , 2005, The Plant journal : for cell and molecular biology.

[30]  J. Brosius,et al.  Retroposons--seeds of evolution. , 1991, Science.

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

[32]  B. Larkins,et al.  A Defective Signal Peptide Tethers the floury-2 Zein to the Endoplasmic Reticulum Membrane , 1997, Plant physiology.

[33]  M. Theodorou,et al.  Phosphate starvation-inducible synthesis of the alpha-subunit of the pyrophosphate-dependent phosphofructokinase in black mustard suspension cells. , 1992, The Journal of biological chemistry.

[34]  R. Wrobel,et al.  Increased expression of the maize immunoglobulin binding protein homolog b-70 in three zein regulatory mutants. , 1991, The Plant cell.

[35]  B. Larkins,et al.  opaque-2 modifiers increase gamma-zein synthesis and alter its spatial distribution in maize endosperm. , 1991, The Plant cell.

[36]  F. Podestá,et al.  The Functional Organization and Control of Plant Respiration , 2006 .

[37]  B. Larkins,et al.  RBR 3 , a member of the retinoblastoma-related family from maize , is regulated by the RBR 1 E 2 F pathway , 2005 .

[38]  B. Larkins,et al.  Phenotypic effects of opaque2 modifier genes in normal maize endosperm , 1995 .

[39]  B. Larkins,et al.  Characterization of the Variability in Lysine Content for Normal and opaque2 Maize Endosperm , 1996 .

[40]  L. Guilloux.  Characterization of novel proteins affected by the o2 mutation and expressed during maize endosperm development , 2022 .

[41]  E. Mertz,et al.  Mutant Gene That Changes Protein Composition and Increases Lysine Content of Maize Endosperm , 1964, Science.

[42]  Richard D. Thompson,et al.  The transcriptional activatorOpaque-2 controls the expression of a cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms , 1996, Molecular and General Genetics MGG.

[43]  B. Larkins,et al.  A Defective Signal Peptide in a 19-kD α-Zein Protein Causes the Unfolded Protein Response and an Opaque Endosperm Phenotype in the Maize De*-B30 Mutant1 , 2004, Plant Physiology.

[44]  B. Larkins,et al.  Zein Storage Proteins , 2009 .

[45]  J. Sheen.  Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. , 1991, The Plant cell.