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. 2000 Jan;154(1):437–446. doi: 10.1093/genetics/154.1.437

Mutator-suppressible alleles of rough sheath1 and liguleless3 in maize reveal multiple mechanisms for suppression.

L Girard 1, M Freeling 1
PMCID: PMC1460886  PMID: 10629001

Abstract

Insertions of Mutator transposons into maize genes can generate suppressible alleles. Mu suppression is when, in the absence of Mu activity, the phenotype of a mutant allele reverts to that of its progenitor. Here we present the characterization of five dominant Mu-suppressible alleles of the knox (knotted1-like homeobox) genes liguleless3 and rough sheath1, which exhibit neomorphic phenotypes in the leaves. RNA blot analysis suggests that Mu suppression affects only the neomorphic aspect of the allele, not the wild-type aspect. Additionally, Mu suppression appears to be exerting its effects at the level of transcription or transcript accumulation. We show that truncated transcripts are produced by three alleles, implying a mechanism for Mu suppression of 5' untranslated region insertion alleles distinct from that which has been described previously. Additionally, it is found that Mu suppression can be caused by at least three different types of Mutator elements. Evidence presented here suggests that whether an allele is suppressible or not may depend upon the site of insertion. We cite previous work on the knox gene kn1, and discuss our results in the context of interactions between Mu-encoded products and the inherently negative regulation of neomorphic liguleless3 and rough sheath1 transcription.

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Selected References

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  1. Barkan A., Martienssen R. A. Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3502–3506. doi: 10.1073/pnas.88.8.3502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bauer P., Crespi M. D., Szécsi J., Allison L. A., Schultze M., Ratet P., Kondorosi E., Kondorosi A. Alfalfa Enod12 genes are differentially regulated during nodule development by Nod factors and Rhizobium invasion. Plant Physiol. 1994 Jun;105(2):585–592. doi: 10.1104/pp.105.2.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradley D., Carpenter R., Sommer H., Hartley N., Coen E. Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell. 1993 Jan 15;72(1):85–95. doi: 10.1016/0092-8674(93)90052-r. [DOI] [PubMed] [Google Scholar]
  4. Campuzano S., Balcells L., Villares R., Carramolino L., García-Alonso L., Modolell J. Excess function hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell. 1986 Jan 31;44(2):303–312. doi: 10.1016/0092-8674(86)90764-6. [DOI] [PubMed] [Google Scholar]
  5. Chandler V. L., Hardeman K. J. The Mu elements of Zea mays. Adv Genet. 1992;30:77–122. doi: 10.1016/s0065-2660(08)60319-3. [DOI] [PubMed] [Google Scholar]
  6. Chomet P., Lisch D., Hardeman K. J., Chandler V. L., Freeling M. Identification of a regulatory transposon that controls the Mutator transposable element system in maize. Genetics. 1991 Sep;129(1):261–270. doi: 10.1093/genetics/129.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dorsett D. Potentiation of a polyadenylylation site by a downstream protein-DNA interaction. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4373–4377. doi: 10.1073/pnas.87.11.4373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Engels W. R., Johnson-Schlitz D. M., Eggleston W. B., Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. doi: 10.1016/0092-8674(90)90016-8. [DOI] [PubMed] [Google Scholar]
  9. Foster T., Veit B., Hake S. Mosaic analysis of the dominant mutant, Gnarley1-R, reveals distinct lateral and transverse signaling pathways during maize leaf development. Development. 1999 Jan;126(2):305–313. doi: 10.1242/dev.126.2.305. [DOI] [PubMed] [Google Scholar]
  10. Fowler J. E., Muehlbauer G. J., Freeling M. Mosaic analysis of the liguleless3 mutant phenotype in maize by coordinate suppression of mutator-insertion alleles. Genetics. 1996 May;143(1):489–503. doi: 10.1093/genetics/143.1.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Freeling M. A conceptual framework for maize leaf development. Dev Biol. 1992 Sep;153(1):44–58. doi: 10.1016/0012-1606(92)90090-4. [DOI] [PubMed] [Google Scholar]
  12. Gasser S. M., Amati B. B., Cardenas M. E., Hofmann J. F. Studies on scaffold attachment sites and their relation to genome function. Int Rev Cytol. 1989;119:57–96. doi: 10.1016/s0074-7696(08)60649-x. [DOI] [PubMed] [Google Scholar]
  13. Geyer P. K., Corces V. G. DNA position-specific repression of transcription by a Drosophila zinc finger protein. Genes Dev. 1992 Oct;6(10):1865–1873. doi: 10.1101/gad.6.10.1865. [DOI] [PubMed] [Google Scholar]
  14. Gierl A., Schwarz-Sommer Z., Saedler H. Molecular interactions between the components of the En-I transposable element system of Zea mays. EMBO J. 1985 Mar;4(3):579–583. doi: 10.1002/j.1460-2075.1985.tb03669.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Greene B., Walko R., Hake S. Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics. 1994 Dec;138(4):1275–1285. doi: 10.1093/genetics/138.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hake S., Vollbrecht E., Freeling M. Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J. 1989 Jan;8(1):15–22. doi: 10.1002/j.1460-2075.1989.tb03343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hershberger R. J., Warren C. A., Walbot V. Mutator activity in maize correlates with the presence and expression of the Mu transposable element Mu9. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10198–10202. doi: 10.1073/pnas.88.22.10198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Holdridge C., Dorsett D. Repression of hsp70 heat shock gene transcription by the suppressor of hairy-wing protein of Drosophila melanogaster. Mol Cell Biol. 1991 Apr;11(4):1894–1900. doi: 10.1128/mcb.11.4.1894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jack J., Dorsett D., Delotto Y., Liu S. Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer. Development. 1991 Nov;113(3):735–747. doi: 10.1242/dev.113.3.735. [DOI] [PubMed] [Google Scholar]
  20. James M. G., Scanlon M. J., Qin M., Robertson D. S., Myers A. M. DNA sequence and transcript analysis of transposon MuA2, a regulator of Mutator transposable element activity in maize. Plant Mol Biol. 1993 Mar;21(6):1181–1185. doi: 10.1007/BF00023614. [DOI] [PubMed] [Google Scholar]
  21. Kim H. Y., Schiefelbein J. W., Raboy V., Furtek D. B., Nelson O. E., Jr RNA splicing permits expression of a maize gene with a defective Suppressor-mutator transposable element insertion in an exon. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5863–5867. doi: 10.1073/pnas.84.16.5863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lisch D., Chomet P., Freeling M. Genetic characterization of the Mutator system in maize: behavior and regulation of Mu transposons in a minimal line. Genetics. 1995 Apr;139(4):1777–1796. doi: 10.1093/genetics/139.4.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lisch D., Girard L., Donlin M., Freeling M. Functional analysis of deletion derivatives of the maize transposon MuDR delineates roles for the MURA and MURB proteins. Genetics. 1999 Jan;151(1):331–341. doi: 10.1093/genetics/151.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Martienssen R., Baron A. Coordinate suppression of mutations caused by Robertson's mutator transposons in maize. Genetics. 1994 Mar;136(3):1157–1170. doi: 10.1093/genetics/136.3.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Muehlbauer G. J., Fowler J. E., Freeling M. Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf. Development. 1997 Dec;124(24):5097–5106. doi: 10.1242/dev.124.24.5097. [DOI] [PubMed] [Google Scholar]
  26. Muehlbauer G. J., Fowler J. E., Girard L., Tyers R., Harper L., Freeling M. Ectopic expression of the maize homeobox gene liguleless3 alters cell fates in the leaf. Plant Physiol. 1999 Feb;119(2):651–662. doi: 10.1104/pp.119.2.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ortiz D. F., Strommer J. N. The Mu1 maize transposable element induces tissue-specific aberrant splicing and polyadenylation in two Adh1 mutants. Mol Cell Biol. 1990 May;10(5):2090–2095. doi: 10.1128/mcb.10.5.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Peacock W. J., Dennis E. S., Gerlach W. L., Sachs M. M., Schwartz D. Insertion and excision of Ds controlling elements in maize. Cold Spring Harb Symp Quant Biol. 1984;49:347–354. doi: 10.1101/sqb.1984.049.01.041. [DOI] [PubMed] [Google Scholar]
  29. Qin M. M., Robertson D. S., Ellingboe A. H. Cloning of the Mutator transposable element MuA2, a putative regulator of somatic mutability of the a1-Mum2 allele in maize. Genetics. 1991 Nov;129(3):845–854. doi: 10.1093/genetics/129.3.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Raboy V., Kim H. Y., Schiefelbein J. W., Nelson-Jr O. E. Deletions in a dspm insert in a maize bronze-1 allele alter RNA processing and gene expression. Genetics. 1989 Jul;122(3):695–703. doi: 10.1093/genetics/122.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Raina R., Cook D., Fedoroff N. Maize Spm transposable element has an enhancer-insensitive promoter. Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6355–6359. doi: 10.1073/pnas.90.13.6355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rutledge B. J., Mortin M. A., Schwarz E., Thierry-Mieg D., Meselson M. Genetic interactions of modifier genes and modifiable alleles in Drosophila melanogaster. Genetics. 1988 Jun;119(2):391–397. doi: 10.1093/genetics/119.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schneeberger R. G., Becraft P. W., Hake S., Freeling M. Ectopic expression of the knox homeo box gene rough sheath1 alters cell fate in the maize leaf. Genes Dev. 1995 Sep 15;9(18):2292–2304. doi: 10.1101/gad.9.18.2292. [DOI] [PubMed] [Google Scholar]
  34. Schneeberger R., Tsiantis M., Freeling M., Langdale J. A. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development. 1998 Aug;125(15):2857–2865. doi: 10.1242/dev.125.15.2857. [DOI] [PubMed] [Google Scholar]
  35. Sieburth L. E., Meyerowitz E. M. Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell. 1997 Mar;9(3):355–365. doi: 10.1105/tpc.9.3.355. [DOI] [PMC free article] [PubMed] [Google Scholar]

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