Abstract
The roles of sterols in plant development are not well understood, but evidence is emerging that they are required for cell division, polarity and patterning by mechanisms that are independent of brassinosteroids, of which they are precursors. Previous evidence shows that two sterol-defective mutants of Arabidopsis thaliana (L.) Heynh., hyd1 and fk hyd2, are defective in root development. Here we show that the HYD1 gene, like the FK gene, is transcriptionally active in both primary and lateral root meristems, though not in the shoot apical meristem. The patterns of cell division during early stages of lateral root initiation in the hyd1 and fk hyd2 mutants appear normal. Previous evidence also suggests that auxin and ethylene signalling is defective in the mutants. Here we show that the cytokinin- and ethylene-responsive ACS1::GUS reporter in the fk hyd2 mutant responds to exogenous cytokinins but not to the ethylene precursor 1-aminocyclopropane-1-carboxylic acid, indicative of normal cytokinin signalling but supporting the hypothesis that ethylene signalling is defective. The defective root meristem cell division activity and expression patterns of the auxin-regulated DR5::GUS and IAA2::GUS reporters can be rescued to a significant extent by the pharmacological or genetic inhibition of ethylene signalling, but not by treatment with aminoethoxyvinylglycine, an inhibitor of ethylene synthesis. This supports the emerging view that the hyd1 and fk hyd2 mutants exhibit an enhanced and unregulated ethylene signalling activity, which accounts for at least part of the observed mutant phenotypes, including disrupted auxin signalling. The possible relationship between ethylene signalling, membrane sterols and meristem function is discussed.
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Abbreviations
- ACC :
-
1-Aminocyclopropane-1-carboxylic acid
- AVG :
-
Aminoethoxyvinylglycine
- BA :
-
N6-Benzyladenine
- GUS :
-
β-Glucuronidase
- RT–PCR :
-
Reverse transcription–polymerase chain reaction
References
Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152
Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero PJ, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171
Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR 1: similarity of product to two-component regulators. Science 262:539–544
Cline MG (1991) Apical dominance. Bot Rev 57:318–358
Clouse SD, Sasse J (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451
Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84
Friml J, Wisniewska J, Benkova E, Mendgen,K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809
Friml J, Benkova E, Mayer U, Palme K, Muster G (2003) Automated whole mount localisation techniques for plant seedlings. Plant J 34:115–124
Fu X, Harberd, NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743
Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428
Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook M, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387
Hall AE, Chen QHG, Findell JL, Schaller GE, Bleecker AB (1999) The relationship between ethylene binding and dominant insensitivity conferred by mutant forms of the ETR1 ethylene receptor. Plant Physiol 121:291–299
Hauser M-T, Bauer E (2000) Histochemical analysis of root meristem activity in Arabidopsis thaliana using a cyclin:GUS (beta-glucuronidase) marker line. Plant Soil 226:1–10
He J-X, Fujioka S, Li T-S, Kang SG, Seto H, Takatsuto S, Yoshida S, Jang J-C (2003) Sterols regulate development and gene expression in Arabidopsis. Plant Physiol 131:1258–1269
Jang J-C, Fujioka S, Tasaka M, Seto H, Takatsuto S, Ishii A, Aida M, Yoshida S, Sheen J (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev 14:1485–1497
Lauber MH, Wiaznegger I, Steinmann T, Schwartz H, Mayer U, Hwang I, Lukowitz W, Jürgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis specific-syntaxin. J Cell Biol 139:1485–1493
Liang X, Oona Y, Shen NF, Kohler C, Li K, Scolnik PA, Theologis A (1995) Characterisation of two members (ACS1 and ACS3) of the 1-aminocyclopropane-1-carboxylase synthase gene family of Arabidopsis thaliana. Gene 167:17–24
Lieberman M, Kunishi AT, Owens LD (1975) Specific inhibitors of ethylene production as retardants of the ripening process in fruits. In: Ulrich R (ed) Facteurs et regulation de la maturation des fruits. Colloq Int CNRS 238:161–170
Lindsey K, Casson S, Chilley P (2002) Peptides: new signalling molecules in plants. Trends Plant Sci 7:78–83
Lindsey K, Topping JF, Pullen ML (2003) Importance of plant sterols in pattern formation and hormone signalling. Trends Plant Sci 8:521–525
Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69:461–476
Rodrigues-Pousada R, Van Caeneghem W, Chauvaux N, Van Onekelen H, Van Montagu M, Van Der Straeten D (1999) Hormonal cross-talk regulates the Arabidopsis thaliana 1-aminocyclopropane-1-carboxylate synthase gene 1 in a developmental and tissue-dependent manner. Physiol Plant 105:312–320
Rodriguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleeker AB (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998
Ryan CA, Pearce G, Scheer JM, Moura, DS (2002) Polypeptide hormones. Plant Cell [Suppl] 14:251–264
Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472
Schaller H (2003) The role of sterols in plant growth and development. Prog Lipid Res 42:163–175
Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120:2475–2487
Scheres B, Di Laurenzio L, Willemsen V, Hauser M-T, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121:53–62
Schrick K, Mayer U, Horrichs A, Kuhnt C, Bellini C, Dangl J, Schmidt J, Jürgens G (2000) FACKEL is a sterol C-14 reductase required for organized cell expansion in Arabidopsis embryogenesis. Genes Dev 14:1471–1484
Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45:527–544
Souter MA, Topping JF, Pullen M, Friml J, Palme K, Hackett R, Grierson D, Lindsey K (2002) hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14:1017–1031
Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653
Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948
Topping JF, May VJ, Muskett PR, Lindsey K (1997) Mutations in the HYDRA1 gene of Arabidopsis perturb cell shape and disrupt embryonic and seedling morphogenesis. Development 124:4415–4424
Vogel JP, Woeste KE, Theologis A, Kieber JJ (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc Natl Acad Sci USA 95:4766–4771
Wei W, Twell D, Lindsey K (1997) A novel nucleic acid helicase gene identified by promoter trapping in Arabidopsis. Plant J 11:1307–1314
Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROLMETHYLTRANSFERASE1 function. Plant Cell 15:612–625
Acknowledgements
We are grateful to the Biotechnology and Biological Sciences Research Council (BBSRC) and the University of Durham for funding studentships to M.A.S. and M.L.P. respectively, and to Huazhong University for a Distinguished Visiting Scholar Felllowship to X.Z. J.F.T. was funded by the European Union (QLK5-CT-1999-01501). We thank Dr. Alan Marchant (University of Nottingham) for providing the IAA2::GUS gene, Dr. Jane Murfett (University of Missouri) for providing DR5::GUS seed, and Dr. D. Van Der Straeten (University of Gent) for providing ACS1::GUS seed.
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Souter, M.A., Pullen, M.L., Topping, J.F. et al. Rescue of defective auxin-mediated gene expression and root meristem function by inhibition of ethylene signalling in sterol biosynthesis mutants of Arabidopsis . Planta 219, 773–783 (2004). https://doi.org/10.1007/s00425-004-1280-z
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DOI: https://doi.org/10.1007/s00425-004-1280-z