Skip to main content
SpringerLink
Log in

Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain α-,ω-dicarboxylic fatty acids and formation of extracellular matrix

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

Abstract

In plants, extracellular matrix polymers built from polysaccharides and cuticular lipids have structural and protective functions. The cuticle is found to be ten times thinner in Arabidopsis thaliana (L.) Heynh than in many other plants, and there is evidence that it is unusual in having a high content of α-,ω-dicarboxylic fatty acids (FAs) in its polyesters. We designated the new organ fusion mutant hth-12 after it appeared to be allelic to adhesion of calyx edges (ace) and hothead (hth), upon molecular cloning of the gene by transposon tagging. This mutant is deficient in its ability to oxidize long-chain ω-hydroxy FAs to ω-oxo FAs, which results in leaf polyesters in decreased α-,ω-dicarboxylic FAs and increased ω-hydroxy FAs. These chemical phenotypes lead to disorder of the cuticle membrane structure in hth-12. ACE/HTH is a single-domain protein showing sequence similarity to long-chain FA ω-alcohol dehydrogenases from Candida species, and we hypothesize that it may catalyze the next step after cytochrome P450 FA ω-hydroxylases in the ω-oxidation pathway. We show that ACE/HTH is specifically expressed in epidermal cells. It appears very likely therefore that the changes in the amount of α-,ω-dicarboxylic FAs in hth-12 reflect the different composition of cuticular polyesters. The ACE/HTH gene is also expressed in root epidermal cells which do not form a polyester membrane on the exterior surface, thereby making it possible that the end products of the pathway, α-,ω-dicarboxylic FAs, are generally required for the cross-linking that ensures the integrity of the outer epidermal cell wall.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

GC–MS:

Gas chromatography–mass spectrometry

RT-PCR:

Reverse transcription-polymerase chain reaction

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscopy

WT:

Wild type

References

  • Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16:2463–2480

    Article  PubMed  CAS  Google Scholar 

  • Agrawal VP, Kolattukudy PE (1977) Biochemistry of suberization: ω-hydroxyacid oxidation in enzyme preparations from suberizing potato tuber disks. Plant Physiol 59:667–672

    Article  PubMed  CAS  Google Scholar 

  • Andrews J, Adams SR, Burton KS, Evered EC (2002) Subcellular localization of peroxidase in tomato fruit skin and the possible implications for the regulation of fruit growth. J Exp Bot 53:2175–2191

    Google Scholar 

  • Araki T, Nakatani-Goto M (1999) Arabidopsis ADHESION OF CALYX EDGES (ACE), genomic. Published only in DataBase

  • Baud S, Bellec Y, Miquel M, Bellini C, Caboche M, Lepiniec L, Faure J-D, Rochat C (2004) gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. EMBO Rep 5:515–520

    Article  PubMed  CAS  Google Scholar 

  • Bellec Y, Harrar Y, Butaeye C, Darnet S, Bellini C, Faure J-D (2002) PASTICCINO2 is a protein tyrosine phosphatase-like involved in cell proliferation and differentiation in Arabidopsis. Plant J 32:713–722

    Article  PubMed  CAS  Google Scholar 

  • Bonaventure G, Beisson F, Ohlrogge J, Pollard M (2004) Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6, cis-9-diene-1,18-dioate as the major component. Plant J 40:920–930

    Article  PubMed  CAS  Google Scholar 

  • Branen JK, Chiou T-J, Engeseth NJ (2001) Overexpression of acyl carrier protein-1 alters fatty acid composition of leaf tissue in Arabidopsis. Plant Physiol 127:222–229

    Article  PubMed  CAS  Google Scholar 

  • Broun P, Poindexter P, Osborne E, Jiang C-Z, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101:4706–4711

    Article  PubMed  CAS  Google Scholar 

  • Browse J, McCourt PJ, Somerville CR (1986) Fatty acid composition of leaf lipids determined after combined digestion and fatty acid methyl ester formation from fresh tissue. Anal Biochem 152:141–145

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15:1170–1185

    Article  PubMed  CAS  Google Scholar 

  • Cheng Q, Liu H-T, Bombelli P, Smith A, Slabas AR (2004) Functional identification of AtFao3, a membrane bound long chain alcohol oxidase in Arabidopsis thaliana. FEBS Lett 574:62–68

    Article  PubMed  CAS  Google Scholar 

  • Dreveny I, Gruber K, Glieder A, Thompson A, Kratky C (2001) The hydroxynitrile lyase from almond: a lyase that looks like an oxidoreductase. Structure 9:803–815

    Article  PubMed  CAS  Google Scholar 

  • Efremova N, Schreiber L, Bär S, Heidmann I, Huijser P, Wellesen K, Schwarz-Sommer Z, Saedler H, Yephremov A (2004) Functional conservation and maintenance of expression pattern of FIDDLEHEAD-like genes in Arabidopsis and Antirrhinum. Plant Mol Biol 56:821–837

    Article  PubMed  CAS  Google Scholar 

  • Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L (2005) Apoplastic polyesters in Arabidopsis surface tissues—a typical suberin and a particular cutin. Phytochemistry 66:2643–2658

    Article  PubMed  CAS  Google Scholar 

  • Haberer G, Erschadi S, Torres-Ruiz RA (2002) The Arabidopsis gene PEPINO/PASTICCINO2 is required for proliferation control of meristematic and non-meristematic cells and encodes a putative anti-phosphatase. Dev Genes Evol 212:542–550

    Article  PubMed  CAS  Google Scholar 

  • Holmquist B, Vallee BL (1991) Human liver class III alcohol and glutathione dependent formaldehyde dehydrogenase are the same enzyme. Biochem Biophys Res Commun 178:1371–1377

    Article  PubMed  CAS  Google Scholar 

  • Kolattukudy PE (2001a) Cutin from plants. In: Doi Y, Steinbuechel A (eds) Biopolymers: polyesters I—biological systems and biotechnological production, vol. 3a. Wiley, Muenster, Germany, pp. 1–35

    Google Scholar 

  • Kolattukudy PE (2001b) Polyesters in higher plants. In: Babel W, Steinbuechel A (eds) Advances in biochemical engineering biotechnology. Biopolyesters, vol. 71. Springer, Berlin Heidelberg New York, pp. 1–49

    Google Scholar 

  • Kolattukudy PE (2001c) Suberin from plants. In: Doi Y, Steinbuechel A (eds) Biopolymers: polyesters I—biological systems and biotechnological production, vol. 3a. Wiley, Muenster, Germany, pp. 41–68

    Google Scholar 

  • Krolikowski KA, Victor JL, Wagler TN, Lolle SJ, Pruitt RE (2003) Isolation and characterization of the Arabidopsis organ fusion gene HOTHEAD. Plant J 35:501–511

    Article  PubMed  CAS  Google Scholar 

  • Kurata T, Kawabata-Awai C, Sakuradani E, Shimizu S, Okada K, Wada T (2003) The YORE–YORE gene regulates multiple aspects of epidermal cell differentiation in Arabidopsis. Plant J 36:55–66

    Article  PubMed  CAS  Google Scholar 

  • Le Bouquin R, Skrabs M, Kahn R, Benveniste I, Salaün JP, Schreiber L, Durst F, Pinot F (2001) CYP94A5, a new cytochrome P450 from Nicotiana tabacum is able to catalyze the oxidation of fatty acids to the ω-alcohol and to the corresponding diacid. Eur J Biochem 268:3083–3090

    Article  PubMed  CAS  Google Scholar 

  • Lolle SJ, Cheung AY, Sussex IM (1992) Fiddlehead: an Arabidopsis mutant constitutively expressing an organ fusion program that involves interactions between epidermal cells. Dev Biol 152:383–392

    Article  PubMed  CAS  Google Scholar 

  • Lolle SJ, Hsu W, Pruitt RE (1998) Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics 149:607–619

    PubMed  CAS  Google Scholar 

  • Lolle SJ, Victor JL, Young JM, Pruitt RE (2005) Genome-wide non-mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434:505–509

    Article  PubMed  CAS  Google Scholar 

  • Nawrath C (2002) The biopolymers cutin and suberin. In: Somerville C, Meyerowitz E (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville

    Google Scholar 

  • Pruitt RE, Vielle-Calzada JP, Ploense SE, Grossniklaus U, Lolle SJ (2000) FIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme. Proc Natl Acad Sci USA 97:1311–1316

    Article  PubMed  CAS  Google Scholar 

  • Schnurr J, Shockey J, Browse J (2004) The Acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16:629–642

    Article  PubMed  CAS  Google Scholar 

  • Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280

    Article  CAS  Google Scholar 

  • Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy PE, Métraux J-P, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12:721–737

    Article  PubMed  CAS  Google Scholar 

  • Sinha N, Lynch M (1998) Fused organs in the adherent 1 mutation in maize show altered epidermal walls with no perturbations in tissue identities. Planta 206:184–195

    Article  CAS  Google Scholar 

  • Sorensen A-M, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  PubMed  CAS  Google Scholar 

  • Steiner-Lange S, Gremse M, Kuckenberg M, Nissing E, Schaechtele D, Spenrath N, Wolff M, Saedler H, Dekker K (2001) Efficient identification of Arabidopsis knock-out mutants using DNA-arrays of transposon flanking sequences. Plant Biol 3:391–397

    Article  CAS  Google Scholar 

  • Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C, Machida Y (2001) A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 128:4681–4689

    PubMed  CAS  Google Scholar 

  • Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol 43:419–428

    Article  PubMed  CAS  Google Scholar 

  • Tanaka T, Tanaka H, Machida C, Watanabe M, Machida Y (2004) A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J 37:139–146

    Article  PubMed  CAS  Google Scholar 

  • Vanhanen S, West M, Kroon JTM, Lindner Nl, Casey J, Cheng Q, Elborough KM, Slabas AR (2000) A consensus sequence for long-chain fatty-acid alcohol oxidases from Candida identifies a family of genes involved in lipid omega-oxidation in yeast with homologues in plants and bacteria. J Biol Chem 275:4445–4452

    Article  PubMed  CAS  Google Scholar 

  • Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308

    Article  PubMed  CAS  Google Scholar 

  • Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Yephremov A (2001) Functional 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

    Article  PubMed  CAS  Google Scholar 

  • Williamson RE, Burn JE, Hocart CH (2001) Cellulose synthesis: mutational analysis and genomic perspectives using Arabidopsis thaliana. Cell Mol Life Sci 58:1475–1490

    Article  PubMed  CAS  Google Scholar 

  • Wisman E, Cardon GH, Fransz P, Saedler H (1998) The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol Biol 37:989–999

    Article  PubMed  CAS  Google Scholar 

  • Xiao F, Goodwin MS, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou J-M (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J 23:2903–2913

    Article  PubMed  CAS  Google Scholar 

  • Yephremov A, Saedler H (2000) Display and isolation of transposon-flanking sequences starting from genomic DNA or RNA. Plant J 21:495–505

    Article  PubMed  CAS  Google Scholar 

  • Yephremov A, Schreiber L (2005) The dark side of the cell wall: molecular genetics of plant cuticle. Plant Biosyst 139:74–79

    Google Scholar 

  • Yephremov A, Wisman E, Huijser P, Huijser C, Wellesen K, Saedler H (1999) Characterization of the FIDDLEHEAD gene reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell 11:2187–2201

    Article  PubMed  CAS  Google Scholar 

  • Yephremov A, Faust A, Kurdyukov S, Trenkamp S, Nawrath C, Franke R, Wojciechowski T, Efremova N, Voisin D, Toro F, Tietjen K, Schreiber L, Saedler H (2004) Safeguarding the cuticular wall. In: Xth cell wall meeting, Sorrento, 29 August–3 September 2004, Italy, p. 99

Download references

Acknowledgments

Sergey Kurdyukov and Andrea Faust contributed equally to this work. We thank Elmon Schmelzer and Rolf-Dieter Hirtz for helping us with microscopy, Aldona Ratajek-Kuhn for taking care of our plants, and RIKEN for providing cDNA clones for our study. We especially appreciate the criticisms of the manuscript made by Paul Hardy, Paul Schulze-Lefert, Michel Caboche, Christiane Nawrath, and Seth Davis. This work has been supported by a MPG fellowship to S.K., a DFG research grant to L.S., and a Bayer CropScience grant to A.Y.

Author information

Author notes

  1. Sergey Kurdyukov

    Present address: ARC Centre of Excellence for Integrative Legume Research, School of Environmental and Life Sciences, University of Newcastle, University Drive, 2308, Callaghan, NSW, Australia

Authors and Affiliations

  1. Max-Planck-Institut für Züchtungsforschung, Carl von Linné Weg 10, 50829, Cologne, Germany

    Sergey Kurdyukov, Andrea Faust, Sascha Bär, Nadia Efremova, Heinz Saedler & Alexander Yephremov

  2. Bayer AG, Bayer CropScience, Research, Target Research , Building 6240, 40789, Monheim, Germany

    Sandra Trenkamp & Klaus Tietjen

  3. Institut für Zelluläre and Molekulare Botanik, Universität Bonn, Kirschallee 1, 53115, Bonn, Germany

    Rochus Franke & Lukas Schreiber

Authors
  1. Sergey Kurdyukov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Faust
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sandra Trenkamp
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sascha Bär
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rochus Franke
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nadia Efremova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Klaus Tietjen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lukas Schreiber
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Heinz Saedler
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alexander Yephremov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander Yephremov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kurdyukov, S., Faust, A., Trenkamp, S. et al. Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain α-,ω-dicarboxylic fatty acids and formation of extracellular matrix. Planta 224, 315–329 (2006). https://doi.org/10.1007/s00425-005-0215-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0215-7

Keywords

Search

Navigation