Abstract
In an effort to identify novel regulatory plant genes, conditional overexpression of toxicArabidopsis thaliana gene products inSaccharomyces cerevisiae was evaluated as a genetic selection scheme. The screening method was tested on a fraction of a cDNA expression library and led to the identification of two Arabidopsis cDNA clones that were toxic to yeast; one corresponded to histone H1 and the other to a previously unidentified gene. This new gene, namedATL2, combines a RING-like zinc-binding motif and a putative signal anchor sequence for membrane insertion in the same molecule. Furthermore, inspection of the 3′ untranslated region reveals two types of sequences which appear to be key determinants in rapid transcript decay. Indeed, rapid and transient accumulation of transcript occurs in the presence of a protein synthesis inhibitor and of the growth regulator auxin. These features provide evidence thatATL2 is an early-response gene. Thus,ATL2 represents one of the first early-response plant genes to be described which possesses a distinct regulatory domain; the fact thatATL2 mRNA is induced by auxin suggests that it might have a role during the response of plants to this growth regulator.
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References
Abel S, Oeller PW, Theologies A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci USA 91:326–330
Abel S, Nguyen MD, Chow W, Theologis A (1995)ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase inArabidopsis thaliana. J Biol Chem 270:19093–19099
Anderson JA, Huprikar SS, Kochian LV, Lucas WJ (1992) Functional expression of a probableArabidopsis thaliana potassium channel inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740
Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1993) Current protocols in molecular biology. John Wiley and Sons, New York
Barlow PN, Luisi B, Milner A, Elliot M, Everett R (1994) Structure of the C3HC4 domain by1H-nuclear magnetic resonance spectroscopy. J Mol Biol 237:201–211
Bender J, Fink GR (1994) AFC1, a LAMMER kinase fromArabidopsis thaliana, activates STE12-dependent processes in yeast. Proc Natl Acad Sci USA 91:12105–12109
Berger SL, Piña B, Silverman N, Marcus GA, Agapite J, Regier JL, Triezenberg SL, Guarente L (1992) Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acid activation domains. Cell 70:251–265
Borden KLB, Boddy MN, Lally J, O'Reilly NJ, Martin S, Howe K, Solomon E, Freemont PS (1995) The solution structure of the RING finger domain from the acute promyelocytic leukaemia proto-oncoprotein PML. EMBO J 14:1532–1541
Botstein D, Fink GR (1988) Yeast: an experimental organism for modern biology. Science 240:1439–1443
Bouchard ML, Côte S (1993) TheDrosophila melanogaster developmental genegl encodes a variant zinc-finger-motif protein. Gene 125:205–209
Bowler C, Chua N-H (1994) Emerging themes of plant signal transduction. Plant Cell 6:1529–1541
Burke D, Gasdaska P, Hartwell L (1992) Dominant effects of tubulin overexpression inSaccharomyces cerevisiae. Mol Cell Biol 9:1048–1059
Certa U, Colavito-Shepanski M, Grunstein M (1984) Yeast may not contain histone H1: the only known ‘histone-like’ protein inSaccharomyces cerevisiae is a mitochondrial protein. Nucleic Acids Res 12:7975–7985
Colicelli J, Nicolette C, Birchmeier C, Rodgers L, Riggs M, Wigler M (1991) Expression of three mammalian cDNAs that interfere with RAS function inSaccharomyces cerevisiae. Proc Natl Acad Sci USA 88:2913–2917
Church GM, Gilbert WG (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Deng X-W, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992)COP1, anArabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and Gβ homologous domain. Cell 71:791–801
Elledge SJ, Mulligan JT, Ramer SW, Spottswood M, Davis RW (1991)λYES: A multifunctional cDNA expression vector for the isolation of genes by complementation of yeast andEscherichia coli mutations. Proc Natl Acad Sci USA 88:1731–1735
Espinet C, Torre MAdl, Aldea M, Herrero E (1995) An efficient method to isolate yeast genes causing overexpression-mediated growth arrest. Yeast 1145:25–32
Estruch F, Carlson M (1993) Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant ofSaccharomyces cerevisiae. Mol Cell Biol 13:3872–3881
Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64:483–484
Frommer WB, Ninnemann O (1995) Heterologous expression of genes in bacterial, fungal, animal and plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:419–444
Gantt SG, Lenvik TR (1991)Arbidopsis thaliana H1 histones. Analysis of two members of a small gene family. Eur J Biochem 202:1029–1031
Gietz D, Jean AS, Woods RA, Schiestl RH (1992) Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425
Gil P, Liu Y, Orbovic V, Verkamp E, Poff KL, Green PJ (1994) Characterization of the auxin-inducibleSAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol 104:777–784
Guilfoyle TJ (1986) Auxin-regulated gene expression in higher plants. CRC Crit Rev Plant Sci 4:247–276
Guthrie C, Fink GR (1991) Guide to yeast genetics and molecular biology. Academic Press, San Diego
Hartmann E, Rapoport TA, Lodish HF (1989) Predicting the orientation of eukaryotic membrane-spanning proteins. Proc Natl Acad Sci USA 86:5786–7590
Herschman HR (1991) Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem 60:281–319
Jones JS, Weber S, Prakash L (1988) TheSaccharomyces cerevisiae RAD18 gene encodes a protein that contains potential zinger finger domains for nucleic binding and a putative nucleotide binding sequence. Nucleic Acids Res 16:7119–7131
Kakizuka A, Miller WH, Umesono K, Warrell RP, Frankel SR, Murty VS, Dmitrovsky E, Evans RM (1991) Chromosomal translocationt(15;17) in human acute promyelocytic leukemia fuses RARα with a novel putative transcription factor, PML. Cell 66:663–674
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Leyser HMO, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993)Arabidopsis auxin-resistance geneAXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161–164
Linder C, Thoma F (1994) Histone H1 expressed inSaccharomyces cerevisiae binds to chromatin and affects survival, growth, transcription, and plasmid stability but does not change nucleosomal spacing. Mol Cell Biol 14:2822–2835
Liu H, Krizek J, Bretscher A (1992) Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics 132:665–673
Marcus GA, Silverman N, Berger SL, Horiuchi J, Guarente L (1994) Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J 13:4807–4815
McClure BA, Guilfoyle TJ (1987) Characterization of a class of small auxin-inducible soybean polyadenylated RNAs. Plant Mol Biol 9:611–623
McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ (1989) Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1:229–239
McDowell Mj, Huang S, McKinney EC, An Y-Q, Meagher, RB (1996) Structure and evolution of the actin gene family inArabidopsis thaliana. Genetics 142:587–602
Miki Y et al. (1994) A strong candidate for the breast and ovarian cancer suceptivility geneBRCA1. Science 266:66–71
Miseloshev G, Venkov P, Holde Kv, Zlatanova J (1994) Low levels of exogenous histone H1 in yeast cause cell death. Proc Natl Acad Sci USA 91:11567–11570
Nakai K, Kanehisa M (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897–911
Nasr F, Bertauche N, Dufour ME, Minet M, Lacroute F (1994) Heterospecific cloning ofArabidopsis thaliana cDNAs by direct complementation of pyrimidine auxotrophic mutants ofSaccharomyces cerevisiae. I. Cloning and sequence analysis of two cDNAs catalysing the second, fifth and sixth steps of the de novo pyrimidine biosynthesis pathway. Mol Gen Genet 244:23–32
Newman TC, Ohme-Takagi M, Taylor CB, Green PJ (1993) DST sequences, highly conserved among plantSAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5:701–714
Ohme-Takagi M, Taylor CB, Newman TC, Green PJ (1993) The effect of sequences with high AU content on mRNA stability in tobacco. Proc Natl Acad Sci 90:11811–11815
Perry LJ, Rixon FJ, Everett RD, Frame MC, McGeoch DJ (1986) Characterization of theIE110 gene of herpes simplex virus type 1. J Gen Virol 67:2365–2380
Ramer SW, Elledge SJ, Davis RW (1992) Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc Natl Acad Sci USA 89:11589–11593
Robinson LC, Tatchell K (1990) TFS1: a suppresor ofcdc25 mutations inSaccharomyces cerevisiae. Mol Gen Genet 230:241–250
Rose MD, Winston F, Hieter P (1990) Methods in yeast genetics: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Sachs AB (1993) Messenger RNA degradation in eukaryotes. Cells 74:413–421
Schuler MA, Zielinski RE (1989) Methods in plant molecular biology. Academic Press, San Diego
Schena M, Lloyd AM, Davis RW (1993) TheHAT-4 gene ofArabidopsis encodes a developmental regulator. Genes Dev 7:367–379
Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA inSaccharomyces cerevisiae. Genetics 122:19–27
Surdej P, Rield A, Jacobs-Lorena M (1994) Regulation of mRNA stability in development. Annu Rev Genet 28:263–282
Tague BW, Goodman HM (1995) Characterization of a family ofArabidopsis zinc finger protein cDNAs. Plant Mol Biol 28:267–279
Takatduji H, Nakamura N, Katsumoto Y (1994) A new family of zinc finger proteins inPetunia: structure, DNA sequence recognition, and floral organ-specific expression. Plant Cell 6:947–958
Theologis A (1986) Rapid gene regulation by auxin. Annu Rev Plant Physiol 37:407–438
Thomas GJ, Rothstein R (1989) The genetic control of direct-repeat recombination inSaccharomyces: the effect ofrad52 andrad1 on mitotic recombination atGAL10, a transcriptionally regulated gene. Genetics 69:725–738
Tugendreich S, Bassett DE, McKusick VA, Boguski MS, Hieter P (1994) Genes conserved in yeast and humans. Human Mol Genet 3:1509–1517
van der Zaal EJ, Droog FNJ, Boot CJM, Hensgens LAM, Hoge JHC, Schilperoort RA, Libbenga KR (1991) Promoters of auxin-induced genes from tobacco can lead to auxin-inducible and root tip-specific expression. Plant Mol Biol 16:983–998
Wang X, Sato R, Brown MS, Hua X, Goldstein JL (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 77:53–62
Yamamoto KT, Mori H, Imaseki H (1992) cDNA cloning of indole-3-acetic acid-regulated genes: Aux22 and SAUR from mung bean (Vigna radiata) hypocotyl tissue. Plant Cell Physiol 33:93–97
Zlatanova J (1990) Histone H1 and the regulation of transcription of eukaryotic genes. Trends Biochem Sci 273–276
Zubiaga AM, Belasco JG, Greenberg ME (1995) The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol Cell Biol 15:2219–2230
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Martínez-García, M., Garcidueñas-Piña, C. & Guzmán, P. Gene isolation inArabidopsis thaliana by conditional overexpression of cDNAs toxic toSaccharomyces cerevisiae: identification of a novel early response zinc-finger gene. Molec. Gen. Genet. 252, 587–596 (1996). https://doi.org/10.1007/BF02172405
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DOI: https://doi.org/10.1007/BF02172405