Abstract
In Arabidopsis, loss of function of the epidermis-specific FDH gene coding for a putative β-ketoacyl-CoA synthase results in ectopic organ fusions in mutants. Corresponding mutants are not available for Antirrhinum majus, however, organ fusions can be induced in both species by chloroacetamide inhibitors of β-ketoacyl-CoA synthases using a chemical genetics approach. We isolated the ortholog of FDH from Antirrhinum majus, the ANTIRRHINUM FIDDLEHEAD (AFI ) gene, and showed that AFI complements fdh when expressed in the epidermis under control of the FDH promoter. Like FDH, the AFI gene exhibits protodermis- and epidermis-specific expression, and its promoter directs the expression of reporter genes to the epidermis in transgenic Antirrhinum and Arabidopsis. We demonstrate down-regulation of the FDH promoter in the epidermis of the ovary septum, thereby supporting the assumption that FDH-like genes may directly facilitate the cell–cell interactions that need to occur during carpel fusion and pollen tube growth. Up-regulation of FDH in the stomium, on the other hand, provides evidence for its possible involvement in cell separation during anther dehiscence. Down-regulation of the FDH and AFI promoters in the septum is observed in transgenic Arabidopsis but not in Antirrhinum plants. This probably reflects differences in the ontogeny of the ovary septum between the two species. We also show that epidermis-specific FDH-like genes may not be able to efficiently elongate fatty acid chains when misexpressed in seeds.
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References
M. Abe T. Takahashi Y. Komeda (1999) ArticleTitleCloning and characterization of an L1 layer-specific gene in Arabidopsis thaliana Plant Cell Physiol. 40 571–580
D.K. Awasthi V. Kumar Y.S. Murty (1984) ArticleTitleFlower development in Antirrhinum majus L (Scrophulariaceae) with a comment upon corolla tube formation. Bot. Mag. Tokyo 97 13–22
S. Baud Y. Bellec M. Miquel C. Bellini M. Caboche L. Lepiniec J.-D. Faure C. Rochat (2004) ArticleTitleGurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase EMBO Rep. 5 515–520
D. Becker E. Kemper J. Schell R. Masterson (1992) ArticleTitleNew plant binary vectors with selectable markers located proximal to the left T-DNA border Plant Mol. Biol. 20 1195–1197
P. Boeger B. Matthes J. Schmalfuss (2000) ArticleTitleTowards the primary target of chloroacetamides–new findings pave the way Pest Manage. Sci. 56 497–508
X. Chen S.M. Goodwin V.L. Boroff X. Liu M.A. Jenks (2003) ArticleTitleCloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production Plant Cell 15 1170–1185
L. Duret P. Bucher (1997) ArticleTitleSearching for regulatory elements in human noncoding sequences Curr. Opin. Struct. Biol. 7 399–406
N. Efremova M.-C. Perbal A. Yephremov W.A. Hofmann H. Saedler Z. Schwarz-Sommer (2001) ArticleTitleEpidermal control of floral organ identity by class B homeotic genes in Antirrhinum and Arabidopsis Development 128 2661–2671
W.M. Fitch (1970) ArticleTitleDistinguishing homologous from analogous proteins Syst. Zool. 19 99–113
R.B. Goldberg T.P. Beals P.M. Sanders (1993) ArticleTitleAnther development: Basic principles and practical applications Plant Cell 5 1217–1229 Occurrence Handle10.1105/tpc.5.10.1217 Occurrence Handle1:STN:280:ByuC3cfis1Q%3D Occurrence Handle8281038
J. Haseloff K.R. Siemering (1998) The uses of green fluorescent protein in plants M. Chalfie S. Kain (Eds) Green Fluorescent Protein: Properties, Applications, and Protocols John Wiley and Sons Ltd., Chichester, England, 191–220
I. Heidmann N. Efremova H. Saedler Z. Schwarz-Sommer (1998) ArticleTitleA protocol for transformation and regeneration of Antirrhinum majus. Plant J. 13 723–728
M. Huelskamp A. Schnittger (1998) ArticleTitleSpatial regulation of trichome formation in Arabidopsis thaliana. Semin. Cell Devel. Biol. 9 213–220
S. Ishiguro A. Kawai-oda J. Ueda I. Nishida K. Okada (2001) ArticleTitleThe defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis Plant Cell 13 2191–2209 Occurrence Handle10.1105/tpc.13.10.2191 Occurrence Handle1:CAS:528:DC%2BD3MXotVehu7g%3D Occurrence Handle11595796
D.W. James E. Lim J. Keller I. Plooy E. Ralston H.K. Dooner (1995) ArticleTitleDirected tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon Activator Plant Cell 7 309–319
R.A. Jefferson T.A. Kavanagh M.W. Bevan (1987) ArticleTitleGUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants EMBO J. 6 3901–3908
P.D. Jenik V.F. Irish (2000) ArticleTitleRegulation of cell proliferation patterns by homeotic genes during Arabidopsis floral development Development 127 1267–1276
M.K. Kandasamy J.B. Nasrallah M.E. Nasrallah (1994) ArticleTitlePollen-pistil interactions and developmental regulation of pollen tube growth in Arabidopsis Development 120 3405–3418
V. Klimyuk B. Carroll C.M. Thomas J.D. Jones (1993) ArticleTitleAlkali treatment for rapid preparation of plant material for reliable PCR analysis Plant J. 3 493–494
T. Kurata C. Kawabata-Awai E. Sakuradani S. Shimizu K. Okada T. Wada (2003) ArticleTitleThe YORE-YORE gene regulates multiple aspects of epidermal cell differentiation in Arabidopsis Plant J. 36 55–66
C. Lechelt-Kunze R.C. Meissner M. Drewes K. Tietjen (2003) ArticleTitleFlufenacet herbicide treatment phenocopies the fiddlehead mutant in Arabidopsis thaliana Pest Manage. Sci. 59 847–856
K.A. Lennon S. Roy P.K. Hepler E.M. Lord (1998) ArticleTitleThe structure of the transmitting tissue of Arabidopsis thaliana (L.) and the path of pollen tube growth Sex. Plant Reprod. 11 49–59
S.J. Lolle G.P. Berlyn E.M. Engstrom K.A. Krolikowski W.D. Reiter R. E. Pruitt (1997) ArticleTitleDevelopmental regulation of cell interactions in the Arabidopsis fiddlehead-1 mutant: a role for the epidermal cell wall and cuticle Developmental Biol. 189 311–21
S. J. Lolle A. Y. Cheung (1993) ArticleTitlePromiscuous germination and growth of wildtype pollen from Arabidopsis and related species on the shoot of the Arabidopsis mutant fiddlehead Developmental Biol. 155 250–258
S.J. Lolle A.y. Cheung I.M. Sussex (1992) ArticleTitleFiddlehead: an Arabidopsis mutant constitutively expressing an organ fusion program that involves interactions between epidermal cells Developmental Biol. 152 383–392
P. Lu R. Porat J.A. Nadeau D. O’Neill (1996) ArticleTitleIdentification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes Plant Cell 8 2155–2168 Occurrence Handle10.1105/tpc.8.12.2155
A.A. Millar M. Wrischer L. Kunst (1998) ArticleTitleAccumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology Plant Cell 10 1889–1902
M.C. Perbal G. Haughn H. Saedler Z. Schwarz Sommer (1996) ArticleTitleNon-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking Development 122 3433–3441
R.E. Pruitt J.P. Vielle-Calzada S.E. Ploense U. Grossniklaus S.J. Lolle (2000) ArticleTitleFIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme Proc. Natl. Acad. Sci. USA 97 1311–1316
M. Rossak M. Smith L. Kunst (2001) ArticleTitleExpression of the FAE1 gene and FAE1 promoter activity in developing seeds of Arabidopsis thaliana Plant Mol. Biol. 46 717–725
P.M. Sanders A.Q. Bui K. Weterings K.N. McIntire Y.-C. Hsu P.Y. Lee M.T. Truong T.P. Beals R.B. Goldberg (1999) ArticleTitleAnther developmental defects in Arabidopsis thaliana male-sterile mutants Sex. Plant Reprod. 11 297–322
P.M. Sanders Y. Lee Pei C. Biesgen J.D. Boone T.P. Beals E.W. Weiler R.B. Goldberg (2000) ArticleTitleThe Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway Plant Cell 12 1041–1061 Occurrence Handle10.1105/tpc.12.7.1041 Occurrence Handle1:CAS:528:DC%2BD3cXlslygtL4%3D Occurrence Handle10899973
S. Satina (1944) ArticleTitlePericlinal chimeras in Datura in relation to development and structure (A) of the style and stigma (B) of calyx and corolla Am. J. Bot. 31 493–502
R.A. Sessions P.C. Zambryski (1995) ArticleTitleArabidopsis gynoecium structure in the wild type and in ettin mutants Development 121 1519–1532
A. Sessions D. Weigel M.F. Yanofsky (1999) ArticleTitleThe Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia Plant J. 20 259–263
D.R. Smyth J.L. Bowman E.M. Meyerowitz (1990) ArticleTitleEarly flower development in Arabidopsis Plant Cell 2 755–768 Occurrence Handle10.1105/tpc.2.8.755 Occurrence Handle1:STN:280:ByyD3crmslU%3D Occurrence Handle2152125
A. Stintzi J. Browse (2000) ArticleTitleThe Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis Proc. Natl. Acad. Sci. USA 97 10625–10630
S. Trenkamp W. Martin K. Tietjen (2004) ArticleTitleSpecific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides Proc. Natl. Acad. Sci. USA 101 11903–11908
G. Vancanneyt R. Schmidt S.A. O’Connor L. Willmitzer M. Rocha Sosa (1990) ArticleTitleConstruction of an intron-containing marker gene splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation Mol. Gen. Genet. 220 245–250
C. Van Den Berg V. Willemsen G. Hendriks P. Weisbeek B. Scheres (1997) ArticleTitleShort-range control of cell differentiation in the Arabidopsis root meristem Nature 390 287–289
R. Waites A. Hudson (1995) ArticleTitlePHANTASTICA: a gene required for dorsoventrality of leaves in Antirrhinum majus Development 121 2143–2154 Occurrence Handle1:CAS:528:DyaK2MXmsl2lu7k%3D
F. Weberling (1992) Morphology of Flowers and Inflorescences Cambridge Univ. Press Cambridge, UK, N.Y
K. Wellesen F. Durst F. Pinot I. Benveniste K. Nettesheim E. Wisman S. Steiner-Lang H. Saedler A. Yephremov (2001) ArticleTitleFunctional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid ω-hydroxylation in development Proc. Natl. Acad. Sci. USA 98 9694–9699
A. Yephremov E. Wisman P. Huijser C. Huijser K. Wellesen H. Saedler (1999) ArticleTitleCharacterization of the FIDDLEHEAD gene reveals a link between adhesion response and cell differentiation in the epidermis Plant Cell 11 2187–2201
S. Zachgo E. Andrade Silva Particlede P. Motte W. Troebner H. Saedler Z. Schwarz-Sommer (1995) ArticleTitleFunctional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant Development 121 2861–2875
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Efremova, N., Schreiber, L., Bär, S. et al. Functional conservation and maintenance of expression pattern of FIDDLEHEAD-like genes in Arabidopsis and Antirrhinum. Plant Mol Biol 56, 821–837 (2004). https://doi.org/10.1007/s11103-004-5576-y
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DOI: https://doi.org/10.1007/s11103-004-5576-y