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Novel members of a family of AT hook-containing DNA-binding proteins from rice are identified through theirin vitro interaction with consensus target sites of plant and animal homeodomain proteins

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Abstract

The AT hook is an AT-rich DNA-binding domain that occurs three times in mammalian high-mobility-group I/Y chromosomal proteins and has recently also been identified in DNA-binding proteins from plants. We unexpectedly isolated three rice cDNA clones encoding AT hook-containing proteins in an attempt to isolate homeobox cDNA clones by south-western screening of an expression library with known binding sites forArabidopsis and animal homeodomain proteins. One of these clones (Os-PF1) has previously been identified due to the binding of its encoded protein to PE1, acis-acting element from the oat phytochrome promoter. The other two clones represent rewly described cDNA clones, designatedOs-AT1 andOs-AT2. The Os-AT1 and Os-AT2 proteins were found to have the same specificities as Os-PF1 with respect toin vitro binding of wild-type and mutant PE1 versions. However, all three proteins appeared to bind much stronger in south-western assays to two of the rather AT-rich sequences used in our screening than to the PE1 element. In none of the AT hook proteins clear homologies to transcriptional activation domains could be identified, but the N-terminal regions of Os-AT1 and Os-PF1 were found to show similarity to histone H1 chromosomal proteins. Given their structural characteristics it is conceivable that the rice AT hook proteins bind to gene promoter regions as accessory proteins that may alter the accessibility of chromatin to other nuclear factors. Their predominant expression in young and meristematic tissues suggests that the presence of the AT hook proteins may affect the expression of genes that determine the differentiation status of cells.

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References

  1. Ashley CT, Pendleton CG, Jennings WW, Saxena A, Glover CVC: Isolation and sequencing of cDNA clones encodingDrosophila chromosomal protein D1: J Biol Chem 264: 8394–8401 (1989).

    PubMed  Google Scholar 

  2. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Seidmain JG, Struhl K: Current Protocols in Molecular Biology. Greene Publishing Associates, New York (1987).

    Google Scholar 

  3. Bruce WB, Deng X-W, Quail PH: A negatively acting DNA sequence element mediates phytochrome-directed repression ofphyA gene transcription. EMBO J 10: 3015–3024 (1991).

    PubMed  Google Scholar 

  4. Bustin M, Lehn DA, Landsman D: Structural features of the HMG chromosomal proteins and their genes. Biochim Biophys Acta 1049: 231–243 (1990).

    PubMed  Google Scholar 

  5. Desplan C, Theis J, O'Farrell PH: The sequence specificity of homeodomain-DNA interaction. Cell 54: 1081–1090 (1988).

    PubMed  Google Scholar 

  6. Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    PubMed  Google Scholar 

  7. Gantt JS, Key JL: Molecular cloning of a pea H1 histone cDNA. Eur J Biochem 166: 119–125 (1987).

    PubMed  Google Scholar 

  8. Grasser KD: Plant chromosomal high mobility group (HMG) proteins. Plant J 7: 185–192 (1995).

    Article  PubMed  Google Scholar 

  9. Green PJ, Kay SA, Chua N-H: Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of therbcS-3A gene. EMBO J 6: 2543–2549 (1987).

    PubMed  Google Scholar 

  10. Jackson D, Veit B, Hake S: Expression of maizeKNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413 (1994).

    Google Scholar 

  11. Jacobsen K, Laursen NB, Jensen EØ, Marcke RA, Poulsen C, Marcker KA: HMG I-like proteins from leaf and nodule nuclei interact with different AT motifs in soybean nodulin promoters. Plant Cell 2: 85–94 (1990).

    Article  PubMed  Google Scholar 

  12. Johnson KR, Disney JE, Wyatt CR, Reeves R: Expression of mRNAs encoding mammalian chromosomal proteins HMG-I and HMG-Y during cellular proliferation. Exp Cell Res 187: 69–76 (1990).

    Article  PubMed  Google Scholar 

  13. Kalionis B, O'Farrell PH: A universal target sequence is boundin vitro by diverse homeodomains. Mech Devel 113: 57–70 (1993).

    Article  Google Scholar 

  14. Korfhage U, Trezzini GF, Meier I, Hahlbrock K, Somssich I: Plant homeodomain protein involved in transcriptional regulation of a pathogen defense-related gene. Plant Cell 6: 695–708 (1994).

    Article  PubMed  Google Scholar 

  15. Laible G, Natt E, Seguin A, Doerner PW, Lamb CJ: A novel DNA-binding protein with histone H1 and high mobility group protein I/Y domains sandwiching a glutamine-rich tract interacts with an AT rich enhancer element of the beanPAL2 promoter. EMBL accession number U06712 (1994).

  16. Lam E, Benfey PN, Gilmartin PM, Fang RX, Chua N-H: Site-specific mutations alterin vitro binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86: 7890–7894 (1989).

    PubMed  Google Scholar 

  17. Lam E, Kano-Murakami Y, Gilmartin P, Niner B, Chua N-H: A metal-dependent DNA-binding protein interacts with a constitutive element of a light-responsive promoter. Plant Cell 2: 857–866 (1990).

    Article  PubMed  Google Scholar 

  18. Laursen NB, Larsen K, Knudsen JY, Hoffman HJ, Poulsen C, Marcker KA, Jensen EØ: A protein binding AT-rich sequence in the soybean leghemoglobinc3 promoter is a generalcis element that requires proximal DNA elements to stimulate transcription. Plant Cell 6: 659–668 (1994).

    Article  PubMed  Google Scholar 

  19. Laux T, Scheurinck J, Goldberg RB: A soybean embryo cDNA encodes a DNA binding protein with histone and HMG-protein-like domains. Nucl Acids Res 19: 4768 (1991).

    PubMed  Google Scholar 

  20. Manfioletti G, Giancotti V, Bandiera A, Buratti E, Sautière P, Cary P, Crane-Robinson C, Coles B, Goodwin GH: cDNA cloning of the HMGI-C phosphoprotein associated with neoplastic and undifferentiated phenotypes. Nucl Acids Res 19: 6793–6797 (1991).

    PubMed  Google Scholar 

  21. Matsuoka M, Ichikawa H, Saito A, Tada Y, Fujimura T, Kano-Murakami Y: Expression of a rice homeobox gene causes altered morphology of transgenic plants. Plant Cell 5: 1039–1048 (1993).

    Article  PubMed  Google Scholar 

  22. Müller AJ, Grafe R: Isolation and characterization of cell lines ofNicotiana tabacum lacking nitrate reductase. Mol Gen Genet 161: 67–76 (1978).

    Article  Google Scholar 

  23. Nieto-Sotelo J, Ichida A, Quail PH: PF1: An A-T hook-containing DNA binding protein from rice that interacts with a functionally defined d(AT)-rich element in the oat phytochromeA3 gene promoter. Plant Cell 6: 287–301 (1994).

    Article  PubMed  Google Scholar 

  24. Nieto-Sotelo J, Ichida A, Quail PH: Positive factor 1 (PF1) from oat is an HMGY- and H1 histone-like protein that binds a functionally defined AT-rich DNA element in the oat phytochromeA gene (PHYA3) promoter. Nucl Acid Res 22: 1115–1116 (1994).

    Google Scholar 

  25. de Pater BS, van der Mark F, Rueb S, Katagiri F, Chua N-H, Schilperoort RA, Hensgens LAM: The promoter of the rice geneGOS2 is active in various different monocot tissues and binds rice nuclear factor ASF-1. Plant J 2: 837–844 (1992).

    Article  PubMed  Google Scholar 

  26. Pedersen TJ, Arwood LA, Spiker S, Guiltinan MJ, Thompson WF: High mobility group chromosomal proteins bind to AT-rich tracts flanking plant genes. Plant Mol Biol 16: 95–104 (1991).

    PubMed  Google Scholar 

  27. Reeves R, Elton TS, Nissen MS, Lehn D, Johnson KR: Post-transcriptional gene regulation and specific binding of the nonhistone protein HMG-I by the 3′ untranslated region of bovine interleukine 2 cDNA. Proc Natl Acad Sci USA 84: 6531–6535 (1987).

    PubMed  Google Scholar 

  28. Reeves R, Nissen MS: The A·T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. J Biol Chem 265: 8573–8582 (1990).

    PubMed  Google Scholar 

  29. Rey P, Diaz C, Schilperoort RA, Hensgens LAM: Cell-type specific expression of three rice genesGOS2, GOS5 andGOS9. Plant Mol Biol 23: 889–894 (1994).

    Article  Google Scholar 

  30. Rueb S, Leneman M, Schilperoort RA, Hensgens LAM: Efficient plant regeneration through somatic embryogenesis from callus induced on mature rice embryos (Oryza sativa L.). Plant Cell Tiss Org Cult 36: 259–264 (1994).

    Google Scholar 

  31. Sanger F, Nickler S, Coulson AR: DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  32. Schena M, Lloyd AM, Davis RW: TheHAT4 gene ofArabidopsis encodes a developmental regulator. Genes Devel 7: 367–379 (1993).

    PubMed  Google Scholar 

  33. Sessa G, Morelli G, Ruberti I: The Athb-1 and-2 HD-Zip domains homodimerize forming complexes of different DNA binding specificities. EMBO J 12: 3507–3517 (1993).

    PubMed  Google Scholar 

  34. Sinha NR, Williams RE, Hake S: Overexpression of the maize homeobox gene,KNOTTED-1, causes a switch from determinate to indeterminate cell fates. Genes Devel 7: 787–795 (1993).

    PubMed  Google Scholar 

  35. Solomon MJ, Strauss F, Varshavsky A: A mammalian high mobility group protein recognizes any stretch of six A-T base pairs in duplex DNA. Proc Natl Acad Sci USA 83: 1276–1280 (1986).

    PubMed  Google Scholar 

  36. Thanos D, Maniatis T: The high mobility group protein HMG I(Y) is required for NF-κB-dependent virus induction of the humanIFN-β gene. Cell 71: 777–789 (1992).

    Article  PubMed  Google Scholar 

  37. Tjaden G, Coruzzi GM: A novel AT-rich DNA binding protein that combines an HMG I-like DNA binding domain with a putative transcription domain. Plant Cell 6: 107–118 (1994).

    Article  PubMed  Google Scholar 

  38. Tjian R, Maniatis T: Transcriptional activation: a complex puzzle with few easy pieces. Cell 77: 5–8 (1994).

    Article  PubMed  Google Scholar 

  39. Van Slogteren GMS, Hoge JHC, Hooykaas PJJ, Schilperoort RA: Clonal analysis of heterogenous crown gall tumor tissues induced by wild-type and shooter mutant strains ofAgrobacterium tumefaciens: expression of T-DNA genes. Plant Mol Biol 2: 321–333 (1983).

    Google Scholar 

  40. Vinson CR, LaMarco KL, Johnson PF, Landschulz WH, McKnight SL:In situ detection of sequence-specific DNA binding activity specified by a recombinant bacteriophage. Genes Devel 2: 801–806 (1988).

    Google Scholar 

  41. Webster CI, Packman LC, Pwee KH, Knight JS, Gray JC: HMG1 enhances binding of HMGI/Y to a positive regulatory region of the pea plastocyanin promoter. EMBL accession number X89568 (1995).

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  1. Institute of Molecular Plant Sciences, Clusius Laboratory, Leiden University, P.O. Box 9505, 2300 RA, Leiden, The Netherlands

    Annemarie H. Meijer, Erwin L. van Dijk & J. Harry C. Hoge

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  1. Annemarie H. Meijer
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Meijer, A.H., van Dijk, E.L. & Hoge, J.H.C. Novel members of a family of AT hook-containing DNA-binding proteins from rice are identified through theirin vitro interaction with consensus target sites of plant and animal homeodomain proteins. Plant Mol Biol 31, 607–618 (1996). https://doi.org/10.1007/BF00042233

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