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Ethylene and shoot regeneration: hookless1 modulates de novo shoot organogenesis in Arabidopsis thaliana

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Abstract

We have investigated the role of ethylene in shoot regeneration from cotyledon explants of Arabidopsis thaliana. We examined the ethylene sensitivity of five ecotypes representing both poor and prolific shoot regenerators and identified Dijon-G, a poor regenerator, as an ecotype with dramatically enhanced ethylene sensitivity. However, inhibiting ethylene action with silver nitrate generally reduced shoot organogenesis in ecotypes capable of regeneration. In ecotype Col-0, we found that ethylene-insensitive mutants (etr1-1, ein2-1, ein4, ein7) exhibited reduced shoot regeneration rates, whereas constitutive ethylene response mutants (ctr1-1, ctr1-12) increased the proportion of explants producing shoots. Our experiments with ethylene over-production mutants (eto1, eto2 and eto3) indicate that the ethylene biosynthesis inhibitor gene, ETO1, can act as an inhibitor of shoot regeneration. Pharmacological elevation of ethylene levels was also found to significantly increase the proportion of explants regenerating shoots. We determined that the hookless1 (hls1-1) mutant, a suppressor of the ethylene response phenotypes of ctr1 and eto1 mutants, is capable of dramatically enhancing shoot organogenesis. The effects of ACC and loss of HLS1 function on shoot organogenesis were found to be largely additive.

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References

  • Abeles F, Morgan P, Saltveit M (1992) Ethylene in plant biology, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Armstrong CL, Green CE (1985) Establishment and maintenance of friable, embryogenic maize callus and the involvement of l-proline. Planta 164:207–214

    Article  CAS  Google Scholar 

  • Beyer EM (1979) Effect of silver ion, carbon dioxide, and oxygen on ethylene action and metabolism. Plant Physiol 63:169–173

    Article  PubMed  CAS  Google Scholar 

  • Biddington NL (1992) The Influence of ethylene in plant-tissue culture. Plant Growth Regul 11:173–187

    Article  CAS  Google Scholar 

  • Cary AJ, Che P, Howell SH (2002) Developmental events and shoot apical meristem gene expression patterns during shoot development in Arabidopsis thaliana. Plant J 32:867–877

    Article  PubMed  CAS  Google Scholar 

  • Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15:545–559

    Article  PubMed  CAS  Google Scholar 

  • Che P, Gingerich DJ, Lall S, Howell SH (2002) Global and hormone-induced gene expression changes during shoot development in Arabidopsis. Plant Cell 14:2771–2785

    Article  PubMed  CAS  Google Scholar 

  • Che P, Lall S, Nettleton D, Howell SH (2006) Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol 141:620–637

    Article  PubMed  CAS  Google Scholar 

  • Chen YF, Etheridge N, Schaller GE (2005) Ethylene signal transduction. Ann Bot 95:901–915

    Article  PubMed  CAS  Google Scholar 

  • Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KLC, Hussey PJ, Beale M, Ecker JR, Sandberg GK, Lindsey K (2006) The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058–3072

    Article  PubMed  CAS  Google Scholar 

  • Chraibi KM, Latche A, Roustan JP, Fallot J (1991) Stimulation of shoot regeneration from cotyledons of Helianthus annuus by the ethylene inhibitors, silver and cobalt. Plant Cell Reports 10:204–207

    Google Scholar 

  • Christianson ML, Warnick DA (1983) Competence and determination in the process of in vitro shoot organogenesis. Dev Biol 95:288–293

    Article  PubMed  CAS  Google Scholar 

  • Christianson ML, Warnick DA (1985) Temporal requirement for phytohormone balance in the control of organogenesis in vitro. Dev Biol 112:494–497

    Article  CAS  Google Scholar 

  • De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: Tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 46:827–836

    Article  PubMed  CAS  Google Scholar 

  • DeCook R, Lall S, Nettleton D, Howell SH (2006) Genetic regulation of gene expression during shoot development in Arabidopsis. Genetics 172:1155–1164

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Dharmasiri S, Hellmann H, Walker L, Gray WM, Estelle M (2002) AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis cullin AtCUL1 is required for auxin response. Plant Cell 14:421–433

    Article  PubMed  CAS  Google Scholar 

  • Eliasson L, Bertell G, Bolander E (1989) Inhibitory action of auxin on root elongation not mediated by ethylene. Plant Physiol 91:310–314

    PubMed  CAS  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  PubMed  CAS  Google Scholar 

  • Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677

    Article  PubMed  CAS  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Article  PubMed  CAS  Google Scholar 

  • Hamant O, Nogue F, Belles-Boix E, Jublot D, Grandjean O, Traas J, Pautot V (2002) The KNAT2 homeodomain protein interacts with ethylene and cytokinin signaling. Plant Physiol 130:657–665

    Article  PubMed  CAS  Google Scholar 

  • Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12:757–770

    Article  PubMed  CAS  Google Scholar 

  • Hicks GS (1994) Shoot induction and organogenesis in vitro—a developmental perspective. In Vitro Cell Dev Biol Plant 30P:10–15

    Google Scholar 

  • Holme IB, Torp AM, Hansen LN, Andersen SB (2004) Quantitative trait loci affecting plant regeneration from protoplasts of Brassica oleracea. Theor Appl Genet 108:1513–1520

    Article  PubMed  CAS  Google Scholar 

  • Hu WW, Gong HB, Pua EC (2006) Modulation of SAMDC expression in Arabidopsis thaliana alters in vitro shoot organogenesis. Physiol Plant 128:740–750

    Article  CAS  Google Scholar 

  • Huxter TJ, Thorpe TA, Reid DM (1981) Shoot initiation in light-grown and dark-grown tobacco callus—the role of ethylene. Physiol Plant 53:319–326

    Article  CAS  Google Scholar 

  • Joo S, Kim WT (2007) A gaseous plant hormone ethylene: the signaling pathway. J Plant Biol 50:109–116

    CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Ann Rev Plant Physiol Plant Mol Biol 44:283–307

    Article  CAS  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene-response pathway in Arabidopsis, encodes a member of the RAF family of protein kinases. Cell 72:427–441

    Article  PubMed  CAS  Google Scholar 

  • Kumar PP, Reid DM, Thorpe TA (1987) The role of ethylene and carbon dioxide in differentiation of shoot buds in excised cotyledons of Pinus radiata in vitro. Physiol Plant 69:244–252

    Article  CAS  Google Scholar 

  • Lall S, Nettleton D, DeCook R, Che P, Howell SH (2004) Quantitative trait loci associated with adventitious shoot formation in tissue culture and the program of shoot development in Arabidopsis. Genetics 167:1883–1892

    Article  PubMed  CAS  Google Scholar 

  • Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194

    Article  PubMed  CAS  Google Scholar 

  • Leyser HMO, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161–164

    Article  PubMed  CAS  Google Scholar 

  • Li H, Johnson P, Stepanova A, Alonso JM, Ecker JR (2004) Convergence of signaling pathways in the control of differential cell growth in Arabidopsis. Dev Cell 7:193–204

    Article  PubMed  CAS  Google Scholar 

  • Lincoln C, Britton JH, Estelle M (1990) Growth and development of the AXR1 mutants of Arabidopsis. Plant Cell 2:1071–1080

    Article  PubMed  CAS  Google Scholar 

  • Mano Y, Komatsuda T (2002) Identification of QTLs controlling tissue-culture traits in barley (Hordeum vulgare L.). Theor Appl Genet 105:708–715

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • Nishimura A, Ashikari M, Lin S, Takashi T, Angeles ER, Yamamoto T, Matsuoka M (2005) Isolation of a rice regeneration quantitative trait loci gene and its application to transformation systems. Proc Natl Acad Sci USA 102:11940–11944

    Article  PubMed  CAS  Google Scholar 

  • Ohto MA, Hayashi S, Sawa S, Hashimoto-Ohta A, Nakamura K (2006) Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. Plant Cell Physiol 47:1603–1611

    Article  PubMed  CAS  Google Scholar 

  • Park JE, Kim YS, Yoon HK, Park CM (2007) Functional characterization of a small auxin-up RNA gene in apical hook development in Arabidopsis. Plant Sci 172:150–157

    Article  CAS  Google Scholar 

  • Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115:679–689

    Article  PubMed  CAS  Google Scholar 

  • Pua EC, Chi GL (1993) De novo shoot morphogenesis and plant growth of mustard (Brassica juncea) in vitro in relation to ethylene. Physiol Plant 88:467–474

    Article  CAS  Google Scholar 

  • Pua EC, Lee JEE (1995) Enhanced de novo shoot morphogenesis in vitro by expression of antisense 1-aminocyclopropane-1-carboxylate oxidase gene in transgenic mustard plants. Planta 196:69–76

    Article  CAS  Google Scholar 

  • Qu X, Hall BP, Gao ZY, Schaller GE (2007) A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptors ETR1 and ERS1. BMC Plant Biol 7:3

    Article  PubMed  CAS  Google Scholar 

  • Schiantarelli E, De la Pena A, Candela M (2001) Use of recombinant inbred lines (RILs) to identify, locate and map major genes and quantitative trait loci involved with in vitro regeneration ability in Arabidopsis thaliana. Theor Appl Genet 102:335–341

    Article  CAS  Google Scholar 

  • Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128

    PubMed  CAS  Google Scholar 

  • Skoog P, Miller C (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 54:118–130

    PubMed  CAS  Google Scholar 

  • Souter MA, Pullen ML, Topping JF, Zhang X, Lindsey K (2004) 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

    Article  PubMed  CAS  Google Scholar 

  • Sugiyama M (1999) Organogenesis in vitro. Curr Opin Plant Biol 2:61–64

    Article  PubMed  CAS  Google Scholar 

  • Sussex IM (1954) Experiments on the cause of dorsiventrality in leaves. Nature 174:351–352

    Article  Google Scholar 

  • Taguchi-Shiobara F, Yamamoto T, Yano M, Oka S (2006) Mapping QTLs that control the performance of rice tissue culture and evaluation of derived near-isogenic lines. Theor Appl Genet 112:968–976

    Article  PubMed  CAS  Google Scholar 

  • Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000

    Article  PubMed  CAS  Google Scholar 

  • Valvekens D, Vanmontagu M, Vanlijsebettens M (1988) Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants using kanamycin selection. Proc Natl Acad Sci USA 85:5536–5540

    Article  PubMed  CAS  Google Scholar 

  • Vasil V, Hildebrandt AC (1965) Growth and tissue formation from single, isolated tobacco cells in microculture. Science 145:1454–1455

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  Google Scholar 

  • Wang KLC, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950

    Article  PubMed  CAS  Google Scholar 

  • Yoshida H, Nagata M, Saito K, Wang KLC, Ecker JR (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol 5:14

    Article  PubMed  CAS  Google Scholar 

  • Zhang SB, Lemaux PG (2004) Molecular analysis of in vitro shoot organogenesis. Crit Rev Plant Sci 23:325–335

    Article  CAS  Google Scholar 

  • Zhao QH, Fisher R, Auer C (2002) Developmental phases and STM expression during Arabidopsis shoot organogenesis. Plant Growth Reg 37:223–231

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by an Ontario Premier’s Research Excellence Award (to MNR) and grants from the Ontario Ministry of Agriculture and the Natural Sciences and Engineering Research Council of Canada. Mutant seed stocks were supplied by the Arabidopsis Biological Resource Centre, OH (US). We thank Michael Pautler for his critical reading of this manuscript.

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Correspondence to Manish N. Raizada.

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Communicated by M. Jordan.

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Chatfield, S.P., Raizada, M.N. Ethylene and shoot regeneration: hookless1 modulates de novo shoot organogenesis in Arabidopsis thaliana . Plant Cell Rep 27, 655–666 (2008). https://doi.org/10.1007/s00299-007-0496-3

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