The Zea mays mutants opaque-2 and opaque-7 disclose extensive changes in endosperm metabolism as revealed by protein, amino acid, and transcriptome-wide analyses

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Hartings, Hans ^a   Lauria, Massimiliano ^a   Lazzaroni, Nadia ^a   Pirona, Raul ^a   Motto, Mario ^a  

^a Unità di Ricerca per la Maiscoltura CRA MAC   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FATTY ACID; LIPID; TRANSCRIPTOME; VEGETABLE PROTEIN; DNA BINDING PROTEIN; OPAQUE 2 PROTEIN, ZEA MAYS; OPAQUE-2 PROTEIN, ZEA MAYS; TRANSCRIPTION FACTOR;

AMINO ACID COMPOSITION; AMINO ACID SYNTHESIS; ARTICLE; CARBON METABOLISM; CITRIC ACID CYCLE; DOWN REGULATION; ENDOSPERM; EXPRESSED SEQUENCE TAG; FATTY ACID SYNTHESIS; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC TRANSCRIPTION; GLYCOLYSIS; LIPOGENESIS; MAIZE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPAQUE 2 GENE; OPAQUE 7 GENE; PLANT GENE; PLANT METABOLISM; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; RNA TRANSLATION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; GENETICS; METABOLISM; MUTATION; TRANSGENIC PLANT;

ZEA MAYS;

AMINO ACIDS; DNA-BINDING PROTEINS; ENDOSPERM; GENE EXPRESSION PROFILING; MUTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS; ZEA MAYS;

EID: 78651444472     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-41     Document Type: Article

References (60)

1. Motto M, Thompson R, Salamini F. Genetic regulation of carbohydrate and protein accumulation in seeds. Cellular and Molecular Biology of Plant Seed Development 1997, Larkins BA, Vasil IK.
2. Olsen OA. Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 2004, 16:214-227.
3. Gibbon BC, Larkins BA. Molecular genetic approaches to developing quality protein maize. Trends Genetics 2005, 21:227-233.
4. Coleman CE, Larkins BA. Prolamines of maize. Seed Proteins 1998, Kluwer Academic Publishers, Dordrecht, The Netherlands, Casey R, Shewry PR.
5. Song R, Messing J. Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 2003, 100:9055-9060. 10.1073/pnas.1032999100, 166437, 12853580.
6. Hannah LC. Starch synthesis in the maize endosperm. Maydica 2005, 50:497-506.
7. Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R. Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 2002, 14:2591-2612. 10.1105/tpc.003905, 151238, 12368507.
8. Pirona R, Hartings H, Lauria M, Rossi V, Motto M. Genetic control of endosperm development and of storage products accumulation in maize seeds. Maydica 2005, 50:515-530.
9. Gavazzi F, Lazzari B, Ciceri P, Gianazza E, Viotti A. Wild-type opaque2 and defective opaque2 polypeptides form complexes in maize endosperm cells and bind the opaque2-zein target site. Plant Physiol 2007, 145:933-945. 10.1104/pp.107.103606, 2048768, 17827273.
10. Brochetto-Braga MR, Leite A, Arruda P. Partial purification and characterization of lysine-oxoglutarate reductase activity in normal and opaque-2 maize endosperms. Plant Physiol 1992, 98:1139-1147. 10.1104/pp.98.3.1139, 1080319, 16668738.
11. Azevedo RA, Arruda P, Turner WL, Lea PJ. The biosynthesis and metabolism of the aspartate derived acids in higher plants. Phytochemistry 1997, 46:395-419. 10.1016/S0031-9422(97)00319-1, 9332022.
12. Motto M, Di Fonzo N, Hartings H, Maddaloni M, Salamini F, Soave C, Thompson R. Regulatory genes affecting maize storage protein synthesis. Oxford Survey Plant Mol Cell Biol 1989, 6:87-114.
13. Zhu T, Budworth P, Chen W, Provart N, Chang HS, Guimil S, Su W, Estes B, Zou G, Wang X. Transcriptional control of nutrient partitioning during rice grain filling. Plant Biotechnol J 2003, 1:59-70. 10.1046/j.1467-7652.2003.00006.x, 17147681.
14. Lai J, Dey N, Kim CS, Bharti AK, Rudd S, Mayer KFX, Larkins BA, Becraft P, Messing J. Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Res 2004, 14:1932-1937. 10.1101/gr.2780504, 524417, 15466291.
15. Verza CN, Rezende e Silva T, Cord Neto G, Nogueira FTS, Fish PH, de Rosa VE, Rebello MM, Vettore AL, Rodrigues da Silva F, Arruda P. Endosperm-preferred expression of maize genes as revealed by transcriptome-wide analysis of expressed sequence taq. Plant Mol Biol 2005, 59:363-374. 10.1007/s11103-005-8924-7, 16247562.
16. Di Fonzo N, Gentinetta E, Salamini F, Soave C. Action of the opaque-7 mutation on the accumulation of storage products in maize endosperm. Plant Sci Let 1979, 14:345-354.
17. Wan Y, Poole RL, Huttly AK, Toscano-Underwood C, Feeney K, Welham S, Gooding MJ, Mills C, Edwards KJ, Shewry PR, Mitchell RAC. Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics 2008, 9:121. 10.1186/1471-2164-9-121, 2292175, 18325108.
18. Luan S. Protein phosphatases in plants. Annu Rev Plant Biol 2003, 54:63-92. 10.1146/annurev.arplant.54.031902.134743, 14502985.
19. Wang X, Larkins BA. Genetic analysis of amino acid accumulation in opaque-2 maize endosperm. Plant Physiol 2001, 125:1766-1777. 10.1104/pp.125.4.1766, 88833, 11299357.
20. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell. 2002, Garland Science, New York, 4.
21. Clarke BC, Hobbs M, Skylas D, Appels R. Genes active in developing wheat endosperm. Funct Integr Genomics 2000, 1:44-55. 10.1007/s101420000008, 11793221.
22. Wurmbach E, Yuen T, Sealfon SC. Focused microarray analysis. Methods 2003, 31:306-316. 10.1016/S1046-2023(03)00161-0, 14597315.
23. Chuaqui RF, Bonner RF, Best CJ, Gillespie JW, Flaig MJ, Hewitt DM, Phillips JL, Krizman DB, Tangrea MA, Ahram M, Linehan WM, Knezevic V, Emmert-Buck MR. Post-analysis follow-up and validation of microarray experiments. Nat Genet 2002, 32:509-514. 10.1038/ng1034, 12454646.
24. Schmidt RJ, Ketudat M, Aukerman MJ, Hoschek G. Opaque-2 is a transcriptional activator that recognizes a specific target site in 22 kD zein genes. Plant Cell 1992, 4:689-700. 10.1105/tpc.4.6.689, 160165, 1392590.
25. Damerval C, Le Guilloux M. Characterization of novel target proteins of the o2 mutation expressed during maize endosperm development. Mol Gen Genet 1998, 257:354-361. 10.1007/s004380050657, 9520270.
26. Maddaloni M, Donini G, Balconi C, Rizzi E, Gallusci P, Forlani F, Lohmer S, Thompson R, Salamini F, Motto M. The transcriptional activator Opaque-2 controls the expression of cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms. Mol Gen Genet 1996, 250:647-654.
27. Mechin V, Thevenot C, Le Guilloux M, Prioul JL, Damerval C. Developmental Analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 2007, 143:1203-1219. 10.1104/pp.106.092148, 1820922, 17237188.
28. Mauri I, Maddaloni M, Lohmer S, Motto M, Salamini F, Thompson R, Martegani E. Functional expression of the transcriptional activator Opaque-2 of Zea mays in transformed yeast. Mol Gen Genet 1993, 241:319-326. 10.1007/BF00284684, 8246886.
29. Hinnebusch AG. Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 2005, 59:407-50. 10.1146/annurev.micro.59.031805.133833, 16153175.
30. Curien G, Biou V, Mas-Droux C, Robert-Genthon M, Ferrer JL, Dumas R. Amino acid biosynthesis: new architectures in allosteric enzymes. Plant Physiol Biochem 2008, 46:325-339. 10.1016/j.plaphy.2007.12.006, 18272376.
31. Coruzzi G, Last R. Amino acids. Molecular biology of plants 2000, Rockville, Maryland, Buchanan B, Gruissem W, Jones R, Am. Soc. Plant Physiol.
32. Galili G, Höfgen R. Metabolic engineering of amino acids and storage proteins in plants. Metabolic Eng 2002, 4:3-11. 2002.
33. Frankard V, Ghislain M, Jacobs M. Two feedback-insensitive enzymes of the aspartate pathway in Nicotiana sylvestris. Plant Physiol 1992, 99:1285-1293. 10.1104/pp.99.4.1285, 1080622, 16669034.
34. Guillet G, Poupart J, Basurco J, De Luca V. Expression of tryptophan decarboxylase and tyrosine decarboxylase genes in tobacco results in altered biochemical and physiological phenotypes. Plant Physiol 2000, 122:933-943. 10.1104/pp.122.3.933, 58930, 10712558.
35. Turpin DH, Weger H, Huppe HC. Interactions between photosynthesis, respiration and nitrogen metabolism. Plant Metabolism 509-524. Longman Singapore Publishers, Singapore, Dennis HT, Turpin DH, Lefebre DD, Layzell DB.
36. Mitchell-Olds T, Pedersen D. The molecular basis of quantitative genetic variation in central and secondary metabolism in Arabidopsis. Genetics 1998, 149:739-747. 1460200, 9611188.
37. Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proc Natl Acad Sci USA 2004, 101:7833-7838. 10.1073/pnas.0402267101, 419692, 15136740.
38. Rademacher T, Haüsler RE, Hirsch HJ, Zhang L, Lipka V, Weie D, Kreuzaler F, Peterhänsel C. An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 2002, 32:25-39. 10.1046/j.1365-313X.2002.01397.x, 12366798.
39. Chapman EJ, Estelle M. Mechanism of auxin-regulated gene expression in plants. Ann Rev Genet 2009, 43:265-285. 10.1146/annurev-genet-102108-134148, 19686081.
40. Müller M, Dues G, Balconi C, Salamini F, Thompson RD. Nitrogen and hormonal responsiveness of the 22 kDa α-zein and b-32 genes in maize endosperm is displayed in the absence of the transcriptional regulator Opaque-2. The Plant Journal 1997, 12(2):281-291. 10.1046/j.1365-313X.1997.12020281.x, 9301081.
41. Forestan C, Meda S, Varotto S. ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiol 2010, 152:1373-1390. 10.1104/pp.109.150193, 20044449.
42. LeClere S, Schmelz EA, Chourey PS. Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol 2010, 153:306-318. 10.1104/pp.110.155226, 20237017.
43. Coruzzi G, Bush DR. Nitrogen and carbon nutrient and metabolite signling in plants. Plant Physiol 2001, 125:61-64. 10.1104/pp.125.1.61, 1539326, 11154297.
44. Price J, Laxmi A, St Martin SK, Jang JC. Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 2004, 16:2128-2150. 10.1105/tpc.104.022616, 519203, 15273295.
45. Cotelle V, Meek SE, Provan F, Milne FC, Morrice N, MacKintosh C. 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells. EMBO J 2000, 19:2869-2876. 10.1093/emboj/19.12.2869, 203364, 10856232.
46. Segal G, Song R, Messing J. A new opaque variant of maize by a single dominant RNA-interface-inducing transgene. Genetics 2003, 165:387-397. 1462732, 14504244.
47. Pysh LD, Aukerman MJ, Schmidt RJ. OHP1: a maize basic domain/leucine zipper protein that interacts with Opaque 2. Plant Cell 1993, 5:227-236. 10.1105/tpc.5.2.227, 160265, 8453304.
48. Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ. A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque-2. Proc Natl Acad Sci USA 1997, 94:7685-7690. 10.1073/pnas.94.14.7685, 23883, 9207153.
49. Wang Z, Ueda T, Messing J. Characterization of the maize prolamin box-binding factor-1 (PBF-1) and its role in the developmental regulation of the zein multigene family. Gene 1998, 223:321-332. 10.1016/S0378-1119(98)00244-3, 9858759.
50. Dai M, Hu Y, Zhao Y, Liu G, Zhou DX. A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 2007, 144:380-390. 10.1104/pp.107.095737, 1913789, 17351053.
51. Bhat RA, Borst JW, Riehl M, Thompson RD. Interaction of maize Opaque-2 and the transcriptional co-activators GCN5 and ADA2, in the modulation of transcriptional activity. Plant Mol Biol 2004, 55:239-252. 10.1007/s11103-004-0553-z, 15604678.
52. Torres-Schumann S, Ringli C, Heierli D, Amrhein N, Keller B. In vitro binding of the tomato bZIP transcriptional activator VSF-1 to a regulatory element that controls xylem-specific gene expression. Plant J 1996, 9:283-96. 10.1046/j.1365-313X.1996.09030283.x, 8919907.
53. Ciceri P, Gianazza E, Lazzari B, Lippoli G, Genga A, Hoschek G, Schmidt RJ, Viotti A. Phosphorylation of Opaque-2 changes diurnally and impacts its DNA binding activity. Plant Cell 1997, 9:97-108. 10.1105/tpc.9.1.97, 156904, 9014367.
54. Hartings H, Lazzaroni N, Rossi V, Riboldi GR, Thompson RD, Salamini F, Motto M. Molecular analysis of opaque-2 alleles from Zea mays L. reveals the nature of mutational events and the presence of a hypervariable region in the 5' part of the gene. Genet Res Camb 1995, 65:11-19.
55. Balconi C, Rizzi E, Manzocchi L, Soave C, Motto M. Analysis of in vivo and in vitro grown endosperms of high and low protein strains of maize. Plant Sci 1991, 73:1-9.
56. Moreaux T, Landry J. La maturation de grain de mais. Evolution qualitative et quantitative des différentes formes azotées. Physiol Veg 1972, 10:1-18.
57. Righetti PG, Gianazza E, Viotti A, Soave C. Heterogeneity of storage proteins in maize. Planta 1977, 136:115-123.
58. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J. TM4: A Free, Open-Source System for Microarray Data Management and Analysis. BioTechniques 2003, 34:374-378.
59. Kerr MK, Martin M, Churchill GA. Analysis of variance for gene expression microarray data. J Comput Biol 2000, 7:819-837. 10.1089/10665270050514954, 11382364.
60. Wolfinger R, Gibson G, Wolfinger E, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules R. Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 2001, 8:625-637. 10.1089/106652701753307520, 11747616.