Plant Molecular Biology

, Volume 48, Issue 5–6, pp 575–581 | Cite as

QTL analysis of proteome and transcriptome variations for dissecting the genetic architecture of complex traits in maize

  • L. Consoli
  • A. Lefèvre
  • M. Zivy
  • D. de Vienne
  • C. Damerval

Abstract

In this review, we present some studies on genetic analysis of proteome and transcriptome variations, which exemplify new strategies for a better understanding of the molecular and genetic bases of complex traits. A large genetic variability was revealed at the proteome expression level, which raised the possibility to predict phenotypical performance on the basis of gene product variability. This approach yielded limited results, but could be re-newed by extensive identification of proteins now allowed by mass spectrometry. The dissection of the genetic basis of the variation of individual protein amounts proves very powerful to select `candidate' proteins, physiologically relevant for a given phenotypical trait, as shown by a study on the effect of water stress in maize. In order to investigate factors of grain quality in maize, we selected a regulatory locus known to control the expression of several storage protein genes, Opaque-2, and investigated the relationships between variability in zein amount and composition and the molecular polymorphism at this locus. Moreover, a QTL analysis revealed that the variability in Opaque-2 transcript abundance was controlled by several polymorphic trans-acting regulators unlinked to the Opaque-2 structural gene. Such genetic approaches should represent additional tools for physiological analysis of the huge amounts of data generated by transcritome and proteome projects.

molecular polymorphism Opaque-2 proteome QTL transcriptome zein 

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References

  1. Appel, R.D., Vargas, J.R., Palagi, P.M., Walther, D. and Hochstrasser, D.F. 1997. Melanie II: a third-generation software package for analysis of two-dimensional electrophoresis images II. Algorithms. Electrophoresis 18: 2735-2748.Google Scholar
  2. Audic, S. and Claverie, J. 1997. The significance of digital gene expression profiles. Genome Res. 7: 986-995.Google Scholar
  3. Bahrman, N. and Damerval, C. 1989. Linkage relationships of loci controlling protein amounts in maritime pine (Pinus pinaster Ait.). Heredity 63: 267-274.Google Scholar
  4. Burstin, J. and Charcosset, A. 1997. Relationship between phenotypic and marker distances: theoretical and experimental investigations. Heredity 79: 477-483.Google Scholar
  5. Burstin. J., Charcosset, A., Barrière, Y., Hébert, Y., de Vienne, D. and Damerval, C. 1995. Molecular markers and protein quantities as genetic descriptors in maize. II. Prediction of hybrids for forage traits. Plant Breed. 114: 427-433.Google Scholar
  6. Burstin. J., de Vienne, D., Dubreuil, P. and Damerval, C. 1994. Molecular markers and protein quantities as genetic descriptors in maize. I. Genetic diversity among 21 inbred lines. Theor. Appl. Genet. 89: 943-950.Google Scholar
  7. Churchill, G.A. and Doerge, R.W. 1994. Empirical threshold values for quantitative trait mapping. Genetics 138: 963-971.Google Scholar
  8. Consoli. L. 2000. Analyse de la variabilité d'expression et de structure de gènes cibles du facteur de transcription Opaque-2 chez le maïs (Zea mays L.). Recherche d'associations avec le polymorphisme au locus O2. Thèse Doctorat en Sciences, Université Paris XI, Orsay, France, 94 pp.Google Scholar
  9. Consoli, L. and Damerval, C. 2001. Quantification of individual zein isoforms resolved by two-dimensional electrophoresis. Genetic variability in 45 maize inbred line. Electrophoresis 22: 2983-2989.Google Scholar
  10. Cord Neto, G., Yunes, J.A., Da Silva, M.J., Vettore, A.L., Arruda, P. and Leite, A. 1995. The involvement of Opaque 2 on β-prolamin gene regulation in maize and Coix suggests a more general role for this transcriptional activator. Plant Mol. Biol. 27: 1015-1029.Google Scholar
  11. Damerval, C., Hebert, Y. and de Vienne, D. 1987. Is the polymorphism of protein amounts related to phenotypic variability? A comparison of two-dimensional electrophoresis data with morphological traits in maize. Theor. Appl. Genet. 74: 194-202.Google Scholar
  12. Damerval, C., and Le Guilloux, M. 1998. Characterization of novel target proteins of the O2 mutation expressed during maize endosperm development. Molecular and General Genetics 257: 354-361.Google Scholar
  13. Damerval, C., Maurice, A., Josse, J.M. and de Vienne, D. 1994. Quantitative trait loci underlying gene product variation: a novel perspective for analyzing regulation of genome expression. Genetics 137: 289-301.Google Scholar
  14. de Vienne, D., Leonardi, A. and Damerval, C. 1988. Genetic aspects of variation of protein amounts in maize and pea. Electrophoresis 9: 742-750.Google Scholar
  15. de Vienne, D., Leonardi, A., Damerval, C. and Zivy, M. 1999. Genetics of proteome variation for QTL characterization: application to drought-stress responses in maize. J. Exp. Bot. 50: 303-309.Google Scholar
  16. Doebley, J. 1993. Genetics, development and plant evolution. Curr. Opin. Genet. Dev. 3: 865-872.Google Scholar
  17. Ewing, R.M., Kahla, A.B., Poirot, O., Lopez, F., Audic, S. and Claverie, J. 1999. Large-scale statistical analyses of rice ESTs reveal correlated patterns of gene expression. Genome Res. 9: 950-959.Google Scholar
  18. Frova, C. and Gorla, M.S. 1993. Quantitative expression of maize HSPs: genetic dissection and association with thermotolerance. Theor. Appl. Genet. 86: 213-220.Google Scholar
  19. Gevaert. K. and Vandekerckhove, J. 2000. Protein identification methods in proteomics. Electrophoresis 21: 1145-1154.Google Scholar
  20. Gygi, S.P., Rochon, Y., Franza, B.R. and Aebersold, R. 1999. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19: 1720-1730.Google Scholar
  21. Habben. J.E., Kirleis, A.W., Larkins, B.A. 1993. The origin of lysine-containing proteins in opaque-2 maize endosperm. Plant Mol. Biol. 23: 825-838.Google Scholar
  22. Hartings, H., Maddaloni, M., Lazzaroni, N., Di Fonzo, N., Motto, M., Salamini, F., and Thompson, R. 1989. The O2 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO J. 8: 2795-2801.Google Scholar
  23. Henry, A.M. and Damerval, C. 1997. High rates of polymorphism and recombination at the Opaque-2 locus in cultivated maize. Mol. Gen. Genet. 256: 147-157.Google Scholar
  24. Herbert. B. 1999. Advances in protein solubilisation for two-dimensional electrophoresis. Electrophoresis 20: 660-663.Google Scholar
  25. Landry, J. and Delhaye, S. 1996. A simple and rapid procedure for hydrolyzing minute amounts of proteins with alkali. Anal. Biochem. 243: 191-194.Google Scholar
  26. Landry, J., Delhaye, S., Damerval, C. 2000. Improved method for isolating and quantitating α-amino nitrogen as nonprotein, true protein, salt-soluble proteins, zeins, and true glutelins in maize endosperm. Cereal Chem. 77: 620-626.Google Scholar
  27. Lefèvre, A. 2000. Analyse du polymorphisme du gène Opaque-2 chez le maïs (Zea mays L.) et recherche de facteurs génétiques impliqués dans la variation quantitative de son transcrit. Thèse Doctorat en Sciences, Université Paris VI, 87 pp.Google Scholar
  28. Leonardi, A., Damerval, Hébert, Y., Gallais, A. and de Vienne, D. 1991. Association of protein amount polymorphism (PAP) among maize lines with performances of their hybrids. Theor. Appl. Genet. 82: 552-560.Google Scholar
  29. Lohmer. S., Maddaloni, M., Motto, M., Di Fonzo, N., Hartings, H., Salamini, F. and Thompson. R.D. 1991. The maize regulatory locus Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell 5: 65-73.Google Scholar
  30. Maddaloni, M., Donini, G., Balconi, C., Rizzi, E., Gallusci, P., Forlani, F., Lohmer, S., Thompson, R., Salamini, F. and Motto, M. 1996. The transcriptional activator Opaque-2 controls the expression of a cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms. Mol. Gen. Genet. 250: 647-654.Google Scholar
  31. McIntyre, R.J. 1982. Regulatory genes and adaptation. Past, present and future. Evol. Biol. 15: 247-285.Google Scholar
  32. Mertz, E.T., Bates, L.S. and Nelson, O.E. 1964. Mutant gene that changes protein composition and increases lysine content of maize endosperm. Science 145: 279-280.Google Scholar
  33. O'Farell, P.H. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250: 4007-4021.Google Scholar
  34. Patton, W.F. 2000. A thousand points of light: the application of fluorescence detection technologies to two-dimensional gel electrophoresis and proteomics. Electrophoresis 21: 1123-1144.Google Scholar
  35. Rubenstein, I. and Geraghty, D.E. 1986. The genetic organisation of zein. Adv. Cereal Sci. Technol. 8: 297-315.Google Scholar
  36. Schmidt. R.J., Burr, F.A. Aukerman, M.J. and Burr, B. 1990. Maize regulatory gene Opaque-2 encodes a protein with a 'leucinezipper' motif that binds to zein DNA. Proc. Natl. Acad. Sci. USA 87: 46-50.Google Scholar
  37. Schmidt. R.J., Ketudat, M., Aukerman, M.J. and Hoschek, G. 1992. Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4: 689-700.Google Scholar
  38. Wilkins. M.R., Pasquali, C., Appel, R.D., Ou, K., Golaz, O., Sanchez, J.-C., Yan, J.X., Gooley, A.A., Hugues, G., Humphery-Smith, I., Williams, K.L. and Hochstrasser, D.F. 1996. From proteins to proteomes: large-scale protein identification by twodimensional electrophoresis and amino acid analysis. Biotechnology 14: 61-65.Google Scholar
  39. Yates, J.R.I. 1998. Mass spectrometry and the age of the proteome. J. Mass Spectrom. 33: 1-19.Google Scholar
  40. Zhu, T., Budworth, P., Han, B., Brown, D., Chang, H-S., Zou, G.X.W. 2001. Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8300 genes by a high-density olgonucleotide probe array. Plant Physiol. Biochem. 39: 221-242.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • L. Consoli
    • 1
  • A. Lefèvre
    • 1
  • M. Zivy
    • 1
  • D. de Vienne
    • 1
  • C. Damerval
    • 1
  1. 1.Station de Génétique Végétale INRA/INA-PG/UPSLa Ferme du MoulonFrance

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