Skip to main content
Log in

A Ds-insertion mutant of OSH6 (Oryza sativa Homeobox 6) exhibits outgrowth of vestigial leaf-like structures, bracts, in rice

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

OSH6 (Oryza sativa Homeobox6) is an ortholog of lg3 (Liguleless3) in maize. We generated a novel allele, termed OSH6-Ds, by inserting a defective Ds element into the third exon of OSH6, which resulted in a truncated OSH6 mRNA. The truncated mRNA was expressed ectopically in leaf tissues and encoded the N-terminal region of OSH6, which includes the KNOX1 and partial KNOX2 subdomains. This recessive mutant showed outgrowth of bracts or produced leaves at the basal node of the panicle. These phenotypes distinguished it from the OSH6 transgene whose ectopic expression led to a “blade to sheath transformation” phenotype at the midrib region of leaves, similar to that seen in dominant Lg3 mutants. Expression of a similar truncated OSH6 cDNA from the 35S promoter (35S::ΔOSH6) confirmed that the ectopic expression of this product was responsible for the aberrant bract development. These data suggest that OSH6-Ds interferes with a developmental mechanism involved in bract differentiation, especially at the basal nodes of panicles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

kn1:

Knotted1

KNOX:

KNOTTED1-like homeobox

lg3:

Liguleless3

OSH6:

Oryza sativa Homeobox6

TALE HD:

Three amino acid loop extension homeodomain

References

  • Balcells L, Modolell J, Ruiz-Gómez M (1988) A unitary basis for different Hairy-wing mutations of Drosophila melanogaster. EMBO J 7:3899–3906

    PubMed  CAS  Google Scholar 

  • Barkan A, Martienssen RA (1991) Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1. Proc Natl Acad Sci USA 88:227–236

    Article  Google Scholar 

  • Barton MK, Poethig RS (1993) Formation of the shoot apical meristem in Arabidopsis thaliana—an analysis of development in the wild type and in the shoot meristemless mutant. Development 119:823–831

    Google Scholar 

  • Bellaoui M, Pidkowich MS, Samach A, Kushalappa K, Kohalmi SE, Modrusan Z, Crosby WL, Haughn GW (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13:2455–2470

    Article  PubMed  CAS  Google Scholar 

  • Byrne M, Timmermans M, Kidner C, Martienssen RA (2001) Development of leaf shape. Curr Opin Plant Biol 4:38–43

    Article  PubMed  CAS  Google Scholar 

  • Campuzano S, Balcells L, Villares R, Carramolino L, Garcia-Alonso L, Modolell J (1986) Excess function hairy wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell 44:303–312

    Article  PubMed  CAS  Google Scholar 

  • Chen JJ, Janssen BJ, Williams A, Sinha N (1997) A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell 8:1277–1289

    Google Scholar 

  • Chin HG, Choe MS, Lee S-H, Park SH, Park SH, Koo JC, Kim NY, Lee JJ, Oh BG, Yi GH, Kim SC, Choi HC, Cho MJ, Han C-d (1999) Molecular analysis of rice plants harboring an Ac/Ds transposable element-mediated gene trapping system. Plant J 19:615–624

    Article  PubMed  CAS  Google Scholar 

  • Chuck G, Lincoln C, Hake S (1996) BP induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8:1277–1289

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Robbins TP, Almeida J, Hudson A, Carpenter R (1989) Consequences and mechanisms of transposition in Antirrhinum majus. In: Berg DE, Howe MM (Eds) Mobile DNA. American Society of Microbiology, USA, pp 413–436

    Google Scholar 

  • Copeland JW, Nasiadka A, Dietrich BH, Krause HM (1996) Patterning of the Drosophila embryo by a homeodomain-deleted Ftz polypeptide. Nature 379:162–165

    Article  PubMed  CAS  Google Scholar 

  • de Folter S, Immink RGH, Kieffer M, Parˇenicova´ L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS box transcription factors. Plant Cell 17:1424–1433

    Article  PubMed  Google Scholar 

  • Freeling M (1992) A conceptual framework for maize leaf development. Dev Biol 153:44–58

    Article  PubMed  CAS  Google Scholar 

  • Freeling M, Bertrand-Garcia R., Sinha N (1992) Maize mutants and variants altering developmental time and their heterochronic interactions. BioEssays 14:227–236

    Article  PubMed  CAS  Google Scholar 

  • Greene B, Walko R, Hake S (1994) Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. Genetics 138:1275–1285

    PubMed  CAS  Google Scholar 

  • Goodrich J, Puangsomlee P, Martin M, Long D, Meyerowitz EM, Coupland G (1997) A polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386:44–51

    Article  PubMed  CAS  Google Scholar 

  • Hake S, Vollbrecht E, Freeling M (1989) Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J 8:15–22

    PubMed  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • Hiratsu K, Mitsuda N, Matsui K, Ohme-Takagi M (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321:172–178

    Article  PubMed  CAS  Google Scholar 

  • Hoshikawa K (1989) The growing rice plant—an anatomical monograph. 1st edn. Nobunkyo, Tokyo

    Google Scholar 

  • Itoh JI, Hasegawa A, Kitano H, Nagato Y (1998) A recessive heterochronic mutation, plastochron1, shortens the plastochron and elongates the vegetative phase in rice. Plant Cell 10:1511–1522

    Article  PubMed  CAS  Google Scholar 

  • Kawakatsu T, Itoh JI, Miyoshi K, Kurata N, Alvarez N, Veit B, Nagato Y (2006) PLASTOCHRON2 regulates leaf initiation and maturation in rice. Plant Cell 18:612–625

    Article  PubMed  CAS  Google Scholar 

  • Kerstetter R, Vollbrecht E, Lowe B, Veit B, Yamaguchi J, Hake S (1994) Sequence analysis and expression patterns divide the maize knotted1-like homeobox genes into two classes. Plant Cell 6:1877–1887

    Article  PubMed  CAS  Google Scholar 

  • Kerstetter RA, Laudencia-Chingcuanco D, Smith LG, Hake S (1997) Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development 124:3045–3054

    PubMed  CAS  Google Scholar 

  • Kim CM, Piao HL, Park SJ, Chon NS, Je BI, Sun B–Y, Park SH, Park JY, Lee EJ, Kim MJ, Chung WS, Lee KH, Lee YS, Lee JJ, Won YJ, Lee GH, Nam MH, Cha YS, Yun DW, Eun MY, Han C-d (2004) Rapid, large-scale generation of Ds transposant lines and analysis of the Ds insertion sites in ride. Plant J 39:252–263

    Article  PubMed  CAS  Google Scholar 

  • Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119

    PubMed  CAS  Google Scholar 

  • Kubli E (1986) Molecular mechanisms of suppression in Drosophila. Trends Genet 2:204–209

    Article  CAS  Google Scholar 

  • Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  PubMed  CAS  Google Scholar 

  • Long JA, Moan EI, Medford JI, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379:66–69

    Article  PubMed  CAS  Google Scholar 

  • Lu Q, Kamps MP (1996) Selective repression of transcriptional activators by Pbx1 does not require the homeodomain. Proc Natl Acad Sci USA 93:470–474

    Article  PubMed  CAS  Google Scholar 

  • Markel H, Chandler J, Werr W (2002) Translational fusions with the engrailed repressor domain efficiently convert plant transcription factors into dominant-negative functions. Nucleic Acids Res 30:4709–4719

    Article  PubMed  CAS  Google Scholar 

  • Martienssen R, Lippman Z, May B, Ronemus M, Vaughn M (2004) Transposons, tandem repeats, and the silencing of imprinted genes. Cold Spring Harb Symp Quant Biol 69:371–380

    Article  PubMed  CAS  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickening and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  PubMed  CAS  Google Scholar 

  • Miyoshi K, Ahn BO, Kawakatsu T, Ito Y, Itoh J, Nagato Y, Kurata N (2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880

    Article  PubMed  CAS  Google Scholar 

  • Muehlbauer GJ, Fowler JE, Freeling M (1997) Sectors expressing the homeobox gene liguleless3 iplicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf. Development 124:5097–5106

    PubMed  CAS  Google Scholar 

  • Muehlbauer GJ, Fowler JE, Girard L, Tyers R, Harper L, Freeling M (1999) Ectopic expression of the maize homeobox gene liguleless3 alters cell fates in the leaf. Plant Physiol 119:651–662

    Article  PubMed  CAS  Google Scholar 

  • Müller K, Romano N, Gerstner O, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (1995) The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374:727–730

    Article  PubMed  Google Scholar 

  • Muller J, Wang Y, Franzen R, Santi L, Salamini F, Rohde W (2001) In vitro interactions between barley TALE homeodomain proteins suggest a role for protein—protein associations in the regulation of Knox gene function. Plant J 27:13–23

    Article  PubMed  CAS  Google Scholar 

  • Nagasaki H, Sakamoto T, Sato Y, Matsuoka M (2001) Functional analysis of the conserved domains of a rice KNOX homeodomain protein, OSH15. Plant Cell 13:2085–2098

    Article  PubMed  CAS  Google Scholar 

  • Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968

    Article  PubMed  CAS  Google Scholar 

  • Reiser L, Sanchez-Baracaldo P, Hake S (2000) Knots in the family tree: evolutionary relationships and functions of knox homeobox genes. Plant Mol Biol 42:151–166

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto T, Nishimura A, Tamaoki M, Kuba M, Tanaka H, Iwahori S, Matsuoka M (1999) The conserved KNOX domain mediates specificity of tobacco KNOTTED1-type homeodomain proteins. Plant Cell 11:1419–1432

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto T, Kamiya N, Ueguehi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeocomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Sentoku N, Miura Y, Hirochika H, Kitano H, Matsuoka M (1999) Loss-of-function mutations in the rice homeobox gene OSH15 affect the architecture of internodes resulting in dwarf plants. EMBO J 18:992–1002

    Article  PubMed  CAS  Google Scholar 

  • Schneeberger RG, Becraft PW, Hake S, Freeling M (1995) Ectopic expression of the knox homeobox gene rough sheath1 alters cell fate in the maize leaf. Genes Dev 9:2292–2304

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Sato Y, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development. Plant Cell 11:1651–1664

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Sato Y, Matsuoka M (2000) Overexpression of rice OSH genes induces ectopic shoots on leaf sheaths of transgenic rice plants. Dev Biol 220:358–364

    Article  PubMed  CAS  Google Scholar 

  • Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537

    Article  PubMed  CAS  Google Scholar 

  • Shure M, Wessler S, Fedoroff N (1983) Molecular identification and isolation of the Waxy locus in maize. Cell 35:225–233

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smith LG, Greene B, Veit B, Hake S (1992) A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development 116:21–30

    PubMed  CAS  Google Scholar 

  • Smith HMS, Boschke I, Hake S (2002) Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci USA 99:9579–9584

    Article  PubMed  CAS  Google Scholar 

  • Venglat SP, Dumonceaux T, Rozwadowski K, Parnell L, Babic V, Keller W, Martienssen R, Selvaraj G, Datla R (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA 99:4730–4735

    Article  PubMed  CAS  Google Scholar 

  • Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241–243

    Article  PubMed  CAS  Google Scholar 

  • Weil CF, Wessler SR (1990) The effects of plant transposable element insertion on transcription initiation and RNA processing. Annu Rev Plant Physiol Plant Mol Biol 41:527–552

    Article  CAS  Google Scholar 

  • Williams-Carrier RE, Lie YS, Hake S, Lemaux PG (1997) Ectopic expression of the maize kn1 gene phenocopies the Hooded mutant of barley. Development 124:3737–3745

    PubMed  CAS  Google Scholar 

  • Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant (code # CG151) from Crop Functional Genomics Center of the 21st Century Frontier Research Program. This work also was supported by Korea Research Foundation Grant (KRF-2003-015-C00636), BioGreen 21 Program (Rural Development Administration), by Basic Research Fund (NIAB, 06-2-12-7-1), and from the KOSEF/MOST to the Environmental Biotechnology National Core Research Center (R15-2003-012-01001-0). Sung Han Park, Byoung Il Je, Soon Ju Park, and Hai Long Piao are recipients of fellowships of the Brain Korea21 project. We appreciate very much the comments of Dr. David Jackson at the Cold Spring Harbor Lab (USA).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Moo Young Eun or Chang-deok Han.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1 Comparison of

OSH6-Ds mRNA levels between mutants (m/m) and ones (OSH6, m/m) expressing 35S::OSH6 by RT-PCR. RT-PCR analysis was performed to detect the mRNAs of OSH6-Ds (m/m) and 35S::OSH6 (OSH6) in plants of single and double genetic combinations. OSH6-Ds transcripts were examined by RT-PCR using the primer pair 3-4/5-2 shown in Fig. 4a. OSH6 mRNA from 35S::OSH6 was detected using a primer pair 3F/3R shown in Fig. 3a. The locations of these primer sets are shown in Fig. 3a. Actin mRNA was used as a control (TIFF 970 kB)

Supplementary Fig. 2 Phenotypic comparisons of panicle nodes in mutant plants (m/m) expressing

OSH6-Ds and in plants (OSH6, m/m) expressing 35S-OSH6 and OSH6-Ds. Pancle nodes are shown in mature plants of wild type, OSH6-Ds, 35S-OSH6, and OSH-Ds/3 5S-OSH6 plants. Arrows indicate ‘bract-leaf’ (TIFF 3.51 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, S.H., Kim, C.M., Je, B.I. et al. A Ds-insertion mutant of OSH6 (Oryza sativa Homeobox 6) exhibits outgrowth of vestigial leaf-like structures, bracts, in rice. Planta 227, 1–12 (2007). https://doi.org/10.1007/s00425-007-0576-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0576-1

Keywords

Navigation