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Genetics. May 1994; 137(1): 289–301.
PMCID: PMC1205945

Quantitative Trait Loci Underlying Gene Product Variation: A Novel Perspective for Analyzing Regulation of Genome Expression

Abstract

A methodology to dissect the genetic architecture of quantitative variation of numerous gene products simultaneously is proposed. For each individual of a segregating progeny, proteins extracted from a given organ are separated using two-dimensional electrophoresis, and their amounts are estimated with a computer-assisted system for spot quantification. Provided a complete genetic map is available, statistical procedures allow determination of the number, effects and chromosomal locations of factors controlling the amounts of individual proteins. This approach was applied to anonymous proteins of etiolated coleoptiles of maize, in an F(2) progeny between two distant lines. The genetic map included both restriction fragment length polymorphism and protein markers. Minimum estimates of one to five unlinked regulatory factors were found for 42 of the 72 proteins analyzed, with a large diversity of effects. Dominance and epistasis interactions were involved in the control of 38% and 14% of the 72 proteins, respectively. Such a methodology might help understanding the architecture of regulatory networks and the possible adaptive or phenotypic significance of the polymorphism of the genes involved.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Allendorf FW, Knudsen KL, Phelps SR. Identification of a gene regulating the tissue expression of a phosphoglucomutase locus in rainbow trout. Genetics. 1982 Oct;102(2):259–268. [PMC free article] [PubMed]
  • Artavanis-Tsakonas S. The molecular biology of the Notch locus and the fine tuning of differentiation in Drosophila. Trends Genet. 1988 Apr;4(4):95–100. [PubMed]
  • Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990 Apr 6;61(1):49–59. [PubMed]
  • Bennetzen JL, Swanson J, Taylor WC, Freeling M. DNA insertion in the first intron of maize Adh1 affects message levels: cloning of progenitor and mutant Adh1 alleles. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4125–4128. [PMC free article] [PubMed]
  • Burr B, Burr FA, Thompson KH, Albertson MC, Stuber CW. Gene mapping with recombinant inbreds in maize. Genetics. 1988 Mar;118(3):519–526. [PMC free article] [PubMed]
  • Castle WE. AN IMPROVED METHOD OF ESTIMATING THE NUMBER OF GENETIC FACTORS CONCERNED IN CASES OF BLENDING INHERITANCE. Science. 1921 Sep 9;54(1393):223–223. [PubMed]
  • Chandler VL, Radicella JP, Robbins TP, Chen J, Turks D. Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell. 1989 Dec;1(12):1175–1183. [PMC free article] [PubMed]
  • Church GM, Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. [PMC free article] [PubMed]
  • Conaway RC, Conaway JW. General initiation factors for RNA polymerase II. Annu Rev Biochem. 1993;62:161–190. [PubMed]
  • de Vienne D, Leonardi A, Damerval C. Genetic aspects of variation of protein amounts in maize and pea. Electrophoresis. 1988 Nov;9(11):742–750. [PubMed]
  • Dickinson WJ. Evolution of patterns of gene expression in hawaiian picture-winged Drosophila. J Mol Evol. 1980 Dec;16(2):73–94. [PubMed]
  • Dickinson WJ. On the architecture of regulatory systems: evolutionary insights and implications. Bioessays. 1988 Jun;8(6):204–208. [PubMed]
  • Edwards MD, Stuber CW, Wendel JF. Molecular-marker-facilitated investigations of quantitative-trait loci in maize. I. Numbers, genomic distribution and types of gene action. Genetics. 1987 May;116(1):113–125. [PMC free article] [PubMed]
  • Fang XM, Brennan MD. Multiple cis-acting sequences contribute to evolved regulatory variation for Drosophila Adh genes. Genetics. 1992 Jun;131(2):333–343. [PMC free article] [PubMed]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed]
  • Gardiner JM, Coe EH, Melia-Hancock S, Hoisington DA, Chao S. Development of a core RFLP map in maize using an immortalized F2 population. Genetics. 1993 Jul;134(3):917–930. [PMC free article] [PubMed]
  • Gelbart W, McCarron M, Chovnick A. Extension of the limits of the XDH structural element in Drosophila melanogaster. Genetics. 1976 Oct;84(2):211–232. [PMC free article] [PubMed]
  • Gillespie JH, Kojima K. The degree of polymorphisms in enzymes involved in energy production compared to that in nonspecific enzymes in two Drosophila ananassae populations. Proc Natl Acad Sci U S A. 1968 Oct;61(2):582–585. [PMC free article] [PubMed]
  • Hanson DD, Hamilton DA, Travis JL, Bashe DM, Mascarenhas JP. Characterization of a pollen-specific cDNA clone from Zea mays and its expression. Plant Cell. 1989 Feb;1(2):173–179. [PMC free article] [PubMed]
  • Helentjaris T, Weber D, Wright S. Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. Genetics. 1988 Feb;118(2):353–363. [PMC free article] [PubMed]
  • Johnson GB. Enzyme polymorphism and metabolism. Science. 1974 Apr 5;184(4132):28–37. [PubMed]
  • Jones N. Complex inhibitions. Curr Biol. 1991 Aug;1(4):224–226. [PubMed]
  • Kaelin WG, Jr, Pallas DC, DeCaprio JA, Kaye FJ, Livingston DM. Identification of cellular proteins that can interact specifically with the T/E1A-binding region of the retinoblastoma gene product. Cell. 1991 Feb 8;64(3):521–532. [PubMed]
  • Keim P, Diers BW, Olson TC, Shoemaker RC. RFLP mapping in soybean: association between marker loci and variation in quantitative traits. Genetics. 1990 Nov;126(3):735–742. [PMC free article] [PubMed]
  • Kelly J, Freeling M. Purification of maize alcohol dehydrogenase-1 allozymes and comparison of their tryptic peptides. Biochim Biophys Acta. 1980 Jul 24;624(1):102–110. [PubMed]
  • Lamb P, McKnight SL. Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization. Trends Biochem Sci. 1991 Nov;16(11):417–422. [PubMed]
  • Lander ES, Botstein D. Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics. 1989 Jan;121(1):185–199. [PMC free article] [PubMed]
  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA, Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. [PubMed]
  • Laurie CC, Heath EM, Jacobson JW, Thomson MS. Genetic basis of the difference in alcohol dehydrogenase expression between Drosophila melanogaster and Drosophila simulans. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9674–9678. [PMC free article] [PubMed]
  • Laurie-Ahlberg CC, Bewley GC. Naturally occurring genetic variation affecting the expression of sn-glycerol-3-phosphate dehydrogenase in Drosophila melanogaster. Biochem Genet. 1983 Oct;21(9-10):943–961. [PubMed]
  • Laurie-Ahlberg CC, Maroni G, Bewley GC, Lucchesi JC, Weir BS. Quantitative genetic variation of enzyme activities in natural populations of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1073–1077. [PMC free article] [PubMed]
  • Lebrun M, Freyssinet G. Nucleotide sequence and characterization of a maize cytoplasmic ribosomal protein S11 cDNA. Plant Mol Biol. 1991 Aug;17(2):265–268. [PubMed]
  • Matsuo Y, Yamazaki T. Genetic Analysis of Natural Populations of DROSOPHILA MELANOGASTER in Japan. IV. Natural Selection on the Inducibility, but Not on the Structural Genes, of Amylase Loci. Genetics. 1984 Dec;108(4):879–896. [PMC free article] [PubMed]
  • Miner JN, Yamamoto KR. Regulatory crosstalk at composite response elements. Trends Biochem Sci. 1991 Nov;16(11):423–426. [PubMed]
  • Montoliu L, Rigau J, Puigdomènech P. A tandem of alpha-tubulin genes preferentially expressed in radicular tissues from Zea mays. Plant Mol Biol. 1990 Jan;14(1):1–15. [PubMed]
  • Paterson AH, Lander ES, Hewitt JD, Peterson S, Lincoln SE, Tanksley SD. Resolution of quantitative traits into Mendelian factors by using a complete linkage map of restriction fragment length polymorphisms. Nature. 1988 Oct 20;335(6192):721–726. [PubMed]
  • Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics. 1991 Jan;127(1):181–197. [PMC free article] [PubMed]
  • Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 1987 Dec 1;6(12):3553–3558. [PMC free article] [PubMed]
  • Powell JR, Lichtenfels JM. Population genetics of Drosophila amylase. I. Genetic control of tissue-specific expression in D. pseudoobscura. Genetics. 1979 Jun;92(2):603–612. [PMC free article] [PubMed]
  • Pysh LD, Aukerman MJ, Schmidt RJ. OHP1: a maize basic domain/leucine zipper protein that interacts with opaque2. Plant Cell. 1993 Feb;5(2):227–236. [PMC free article] [PubMed]
  • Rasmussen HH, Van Damme J, Puype M, Gesser B, Celis JE, Vandekerckhove J. Microsequencing of proteins recorded in human two-dimensional gel protein databases. Electrophoresis. 1991 Nov;12(11):873–882. [PubMed]
  • Ruppert S, Boshart M, Bosch FX, Schmid W, Fournier RE, Schütz G. Two genetically defined trans-acting loci coordinately regulate overlapping sets of liver-specific genes. Cell. 1990 Jun 1;61(5):895–904. [PubMed]
  • Skadsen RW, Ruzsa SM, Scandalios JG. Separate molecular mechanisms regulate CAT2 gene expression before and after glyoxysome maturation in two genetic lines of maize. Dev Genet. 1990;11(4):280–288. [PubMed]
  • Smeal T, Angel P, Meek J, Karin M. Different requirements for formation of Jun: Jun and Jun: Fos complexes. Genes Dev. 1989 Dec;3(12B):2091–2100. [PubMed]
  • Thatcher DR. The complete amino acid sequence of three alcohol dehydrogenase alleloenzymes (AdhN-11, AdhS and AdhUF) from the fruitfly Drosophila melanogaster. Biochem J. 1980 Jun 1;187(3):875–883. [PMC free article] [PubMed]
  • Vollbrecht E, Veit B, Sinha N, Hake S. The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature. 1991 Mar 21;350(6315):241–243. [PubMed]
  • Wilson AC, Carlson SS, White TJ. Biochemical evolution. Annu Rev Biochem. 1977;46:573–639. [PubMed]
  • Wilton AN, Laurie-Ahlberg CC, Emigh TH, Curtsinger JW. Naturally occurring enzyme activity variation in Drosophila melanogaster. II. Relationships among enzymes. Genetics. 1982 Oct;102(2):207–221. [PMC free article] [PubMed]
  • Zeng ZB, Houle D, Cockerham CC. How informative is Wright's estimator of the number of genes affecting a quantitative character? Genetics. 1990 Sep;126(1):235–247. [PMC free article] [PubMed]

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