The Gene Balance Hypothesis: Implications for Gene Regulation, Quantitative Traits and Evolution

Overview

Journal New Phytol

Specialty Biology

Date 2009 Nov 21

PMID 19925558

Citations 139

Authors

James A Birchler

Reiner A Veitia

Affiliations

Soon will be listed here.

Abstract

The gene balance hypothesis states that the stoichiometry of members of multisubunit complexes affects the function of the whole because of the kinetics and mode of assembly. Gene regulatory mechanisms also would be governed by these principles. Here, we review the impact of this concept with regard to the effects on the genetics of quantitative traits, the fate of duplication of genes following polyploidization events or segmental duplication, the basis of aneuploid syndromes, the constraints on cis and trans variation in gene regulation and the potential involvement in hybrid incompatibilities.

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References

Schulz C, Tautz D . Autonomous concentration-dependent activation and repression of Krüppel by hunchback in the Drosophila embryo. Development. 1994; 120(10):3043-9. DOI: 10.1242/dev.120.10.3043. View

Maere S, de Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M . Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci U S A. 2005; 102(15):5454-9. PMC: 556253. DOI: 10.1073/pnas.0501102102. View

Dopman E, Hartl D . A portrait of copy-number polymorphism in Drosophila melanogaster. Proc Natl Acad Sci U S A. 2007; 104(50):19920-5. PMC: 2148398. DOI: 10.1073/pnas.0709888104. View

Veitia R . Gene dosage balance in cellular pathways: implications for dominance and gene duplicability. Genetics. 2004; 168(1):569-74. PMC: 1448121. DOI: 10.1534/genetics.104.029785. View

Seidman J, Seidman C . Transcription factor haploinsufficiency: when half a loaf is not enough. J Clin Invest. 2002; 109(4):451-5. PMC: 150881. DOI: 10.1172/JCI15043. View

Birchler J . A study of enzyme activities in a dosage series of the long arm of chromosome one in maize. Genetics. 1979; 92(4):1211-29. PMC: 1214066. DOI: 10.1093/genetics/92.4.1211. View

Rabinow L, Birchler J . A trans-acting regulatory gene that inversely affects the expression of the white, brown and scarlet loci in Drosophila. Genetics. 1991; 129(2):463-80. PMC: 1204636. DOI: 10.1093/genetics/129.2.463. View

Birchler J, Veitia R . The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell. 2007; 19(2):395-402. PMC: 1867330. DOI: 10.1105/tpc.106.049338. View

Devlin R, Holm D, Grigliatti T . The influence of whole-arm trisomy on gene expression in Drosophila. Genetics. 1988; 118(1):87-101. PMC: 1203269. DOI: 10.1093/genetics/118.1.87. View

10.

Yvert G, Brem R, Whittle J, Akey J, Foss E, Smith E . Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet. 2003; 35(1):57-64. DOI: 10.1038/ng1222. View

11.

Sabl J, Birchler J . Dosage dependent modifiers of white alleles in Drosophila melanogaster. Genet Res. 1993; 62(1):15-22. DOI: 10.1017/s0016672300031517. View

12.

Warrior R, Levine M . Dose-dependent regulation of pair-rule stripes by gap proteins and the initiation of segment polarity. Development. 1990; 110(3):759-67. DOI: 10.1242/dev.110.3.759. View

13.

Birchler J, HIEBERT J, Paigen K . Analysis of autosomal dosage compensation involving the alcohol dehydrogenase locus in Drosophila melanogaster. Genetics. 1990; 124(3):679-86. PMC: 1203960. View

14.

Veitia R . Exploring the etiology of haploinsufficiency. Bioessays. 2002; 24(2):175-84. DOI: 10.1002/bies.10023. View

15.

Orr H, Turelli M . The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution. 2001; 55(6):1085-94. DOI: 10.1111/j.0014-3820.2001.tb00628.x. View

16.

Driever W, Nusslein-Volhard C . The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell. 1988; 54(1):95-104. DOI: 10.1016/0092-8674(88)90183-3. View

17.

Lynch M, Conery J . The evolutionary fate and consequences of duplicate genes. Science. 2000; 290(5494):1151-5. DOI: 10.1126/science.290.5494.1151. View

18.

Levine M, Holloway A, Arshad U, Begun D . Pervasive and largely lineage-specific adaptive protein evolution in the dosage compensation complex of Drosophila melanogaster. Genetics. 2007; 177(3):1959-62. PMC: 2147993. DOI: 10.1534/genetics.107.079459. View

19.

Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L . Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr Biol. 2009; 19(13):1128-32. PMC: 6754343. DOI: 10.1016/j.cub.2009.05.068. View

20.

Landry C, Wittkopp P, Taubes C, Ranz J, Clark A, Hartl D . Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics. 2005; 171(4):1813-22. PMC: 1456106. DOI: 10.1534/genetics.105.047449. View