Abstract
The Opaque-2 gene (O2) in maize encodes a transcriptional activator that controls the expression of various genes during kernel development, particularly some of the most abundant endosperm storage protein genes. Compared to its wild relative teosinte, maize has bigger and heavier kernels, with an increased proportion of starch and an altered distribution of the various storage protein categories. The molecular evolution of the O2 gene was investigated in connection with its possible involvement in the domestication process. Most of the coding sequence and parts of introns, 5′UTR, and 3′ noncoding regions were sequenced in a set of cultivated and teosinte accessions. One hundred six polymorphic sites (5.4%) and 72 insertions/deletions, located mostly in noncoding regions, were found. Molecular diversity was quite high (π = 0.0138, θ = 0.0167) compared to that of other transcription factors in maize. The synonymous and nonsynonymous diversity patterns along the coding sequence suggested that different regions are submitted to different functional constraints. Such an evolution would probably be favored by the observed rapid decay of linkage disequilibrium with distance. Cultivated accessions retained about 70% of the diversity observed in teosintes. Purifying selection was detected in both maize and teosintes. No conclusive evidence was obtained for a role of the O2 gene in the domestication process.
Similar content being viewed by others
References
Beadle GW (1939) Teosinte and the origin of maize. J Hered 30:245–247
Causse M, Rocher JP, Henry AM, Charcosset A, Prioul JL, de Vienne D (1995) Genetic dissection of the relationship between carbon metabolism and early growth in maize, with emphasis on key-enzyme loci. Mol Breed 1:259–272
Clark RM, Linton E, Messing J, Doebley JF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci USA 101:700–707
Cord Neto G, Yunes JA, daSilva MJ, Vettore AL, Arruda P, Leite A (1995) The involvement of Opaque 2 on beta-prolamin gene regulation in maize and Coix suggests a more general role for this transcriptional activator. Plant Mol Biol 27:1015–1029
Doebley J (1992) Mapping the genes that made maize. Trends Genet 8:302–307
Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295
Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570
Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346
Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488
Eyre-Walker A, Gaut RL, Hilton H, Feldman DL, Gaut BS (1998) Investigation of the bottleneck leading to the domestication of maize. Proc Natl Acad Sci USA 95:4441–4446
Fay JC, Wu C-I (2000) Hitchhiking under positive darwinian selection. Genetics 155:1405–1413
Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709
Giroux MJ, Boyer C, Feix G, Hannah LC (1994) Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol 106:713–722
Gübitz T, Caldwell A, Hudson A (2003) Rapid molecular evolution of Cycloidea-like genes in Antirrhinum and its relatives. Mol Biol Evol 20:1537–1544
Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hanson MA, Gaut BS, Stec AO, Fuerstenberg SI, Goodman MM, Coe EH, Doebley JF (1996) Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. Genetics 143:1395–1407
Hartings H, Maddaloni M, Lazzaroni N, Fonzo Nd, Motto M, Salamini F, 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
Hartings H, Pirona R, Lazzaroni N, Motto M (2002) Molecular evolution of Opaque-2, a regulatory locus in the genus Zea. Maydica 47:267–275
Henry AM, Damerval C (1997) High rates of polymorphism and recombination at the Opaque-2 locus in cultivated maize. Mol Gen Genet 256:147–157
Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529
Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 120:831–840
Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Järvinen P, Lemmetyinen J, Savolainen O, Sopanen T (2003) DNA sequence variation in BpMADS2 gene in two populations of Betula pendula. Mol Ecol 12:369–384
Kumar S, Tamura K, Jacobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17:1244–1245
Lohmer S, Maddaloni M, Motto M, Di Fonzo N, Hartings H, Salamini F, Thompson RD (1991) The maize regulatory locus Opaque-2 is inhibited by upstream open reading frames present in the leader sequence. Plant Cell 5:65–73
Maddaloni M, Di Fonzo N, Hartings H, Lazzaroni N, Salamini F, Thompson R, Motto M (1989) The sequence of the zein regulatory gene opaque-2 (O2) of Zea mays. Nucleic Acids Res 17:7532
Maddaloni M, Donini G, Balconi C, Rizzi E, Gallusci P, Forlani F, Lohmer S, Thompson R, Salamini F, 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
Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084
Paulis JW, Wall JS (1977) Comparison of protein compositions of selected corns and their wild relatives, teosintes and Tripsacum. Agr Food Chem 25:265–270
Purugganan MD (2000) The molecular population genetics of regulatory genes. Mol Ecol 9:1451–1461
Purugganan MD, Suddith JI (1998) Molecular population genetics of the Arabidopsis CAULIFLOWER regulatory gene: nonneutral evolution and naturally occurring variation in floral homeotic function. Proc Natl Acad Sci USA 95:8130–8134
Purugganan MD, Suddith JI (1999) Molecular population genetics of floral homeotic loci: departures from the equilibrium-neutral model at the APETALA3 and PISTILLATA genes of Arabidopsis thaliana. Genetics 151:839–848
Purugganan MD, Wessler SR (1994) Molecular evolution of the plant R regulatory gene family. Genetics 138:849–854
Purugganan MD, Boyles AL, Suddith JI (2000) Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics 155:855–862
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES IV (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175
Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879–891
Schmidt RJ, Burr FA, Aukerman MJ, Burr B (1990) Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper” motif that binds to zein DNA. Proc Natl Acad Sci USA 87:46–50
Schmidt RJ, Ketudat M, Aukerman MJ, 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
Schmitz D, Lohmer S, Salamini F, Thompson RD (1997) The activation domain of the maize transcription factor Opaque-2 resides in a single acidic region. Nucleic Acids Res 25:756–763
Swofford DL, 2003 PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 40b10. Sinauer Associates, Sunderland, MA
Tajima F, (1983) Evolutionary relationship of DNA sequence in finite populations. Genetics 105:437–460
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley J, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161–9166
Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–80
Tiffin P, Gaut BS (2001) Molecular evolution of the wound-induced serine protease inhibitor wip1 in Zea and related genera. Mol Biol Evol 18:2092–2101
Varagona MJ, Schmidt RJ, Raikhel NV (1992) Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein opaque-2. Plant Cell 4:1213–1227
Vincentz M, Bandeira-Kobarg C, Gauer L, Schlögl P, Leite A (2003) Evolutionary pattern of Angiosperm bZip factors homologous to the maize Opaque2 regulatory protein. J Mol Evo 56:105–116
Wang R-L, Stec A, Hey J, Lukens L, Doebley J (1999) The limits of selection during maize domestication. Nature 398:236–239
Watterson GA, (1975) On the number of segregating sites in genetical models without recombination. Theor Pop Biol 7:256–276
Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B (2004) Cupuliformis establishes lateral organ boudaries in Antirrhinum. Development 131:915–922
White SE, Doebley JF (1999) The molecular evolution of terminal ear1, a regulatory gene in the genus Zea. Genetics 153:1455–1462
Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES IV (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 99:12959–12962
Yunes JA, Cord Neto G, Leite A, Ottoboni LMM, Arruda P (1994a) The role of the Opaque2 transcriptional activator in the regulation of protein accumulation and amino acid metabolism in maize seeds. An Acad Brasil Ci 66:227–237
Yunes JA, Cord Neto G, Silva MJd, Leite A, Ottoboni LMM, Arruda P (1994b) The transcriptional activator Opaque2 recognizes two different target sequences in the 22-kD-like alpha-prolamin genes. Plant Cell 6:237–249
Acknowledgments
We thank Maggie Guilbot, Stéphanie Grenard, and Martine Le Guilloux for technical assistance and Dr. M.I. Tenaillon, O. Panaud, and C. Dillmann for helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
[Reviewing Editor: Dr. Martin Kreitman]
Rights and permissions
About this article
Cite this article
Henry, AM., Manicacci, D., Falque, M. et al. Molecular Evolution of the Opaque-2 Gene in Zea mays L.. J Mol Evol 61, 551–558 (2005). https://doi.org/10.1007/s00239-005-0003-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-005-0003-9