Skip to main content
SpringerLink
Log in

Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells

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

Abstract

Members of the Pinaceae family have complex chemical defense strategies. Conifer defenses associated with specialized cell types of the bark involve constitutive and inducible accumulation of phenolic compounds in polyphenolic phloem parenchyma cells and oleoresin terpenoids in resin ducts. These defenses can protect trees against insect herbivory and fungal colonization. The phytohormone ethylene has been shown to induce the same anatomical and cellular defense responses that occur following insect feeding, mechanical wounding, or fungal inoculation in Douglas fir (Pseudotsuga menziesii) stems (Hudgins and Franceschi in Plant Physiol 135:2134–2149, 2004). However, very little is known about the genes involved in ethylene formation in conifer defense or about the temporal and spatial patterns of their protein expression. The enzyme 1-aminocyclopropane-1-carboxylate oxidase (ACO) catalyzes the final step in ethylene biosynthesis. We cloned full-length and near full-length ACO cDNAs from three conifer species, Sitka spruce (Picea sitchensis), white spruce (P. glauca), and Douglas fir, each with high similarity to Arabidopsis thaliana ACO proteins. Using an Arabidopsis anti-ACO antibody we determined that ACO is constitutively expressed in Douglas fir stem tissues and is up-regulated by mechanical wounding, consistent with the wound-induced increase of ethylene levels. Immunolocalization showed cytosolic ACO is predominantly present in specialized cell types of the wound-induced bark, specifically in epithelial cells of terpenoid-producing cortical resin ducts, in polyphenolic phloem parenchyma cells, and in ray parenchyma cells.

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

Similar content being viewed by others

References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic, San Diego, pp 26–55

    Google Scholar 

  • Alfaro RI (1995) An induced defense reaction in white spruce to attack by the white pine weevil (Pissodes strobi). Can J For Res 25:1725–1730

    Article  Google Scholar 

  • Alfaro RI, Borden JH, King JN, Tomlin ES, McIntosh RL, Bohlmann J (2002) Mechanisms of resistance in conifers against shoot infesting insects. In: Wagner MR, Clancy KM, Lieutier F, Paine TD (eds) Mechanisms and deployment of resistance in trees to insects. Kluwer Academic, Dordrecht, pp 101–126

    Google Scholar 

  • Andersson-Gunneras S, Hellgren JM, Bjorklund S, Regan S, Moritz T, Sundberg B (2003) Asymmetric expression of a poplar ACC oxidase controls ethylene production during gravitational induction of tension wood. Plant J 34:339–349

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  PubMed  CAS  Google Scholar 

  • Bohlmann J, Croteau R (1999) Diversity and variability of terpenoid defenses in conifers: molecular genetics, biochemistry and evolution of the terpene synthase gene family in grand fir (Abies grandis). In: Chadwick DJ, Goode JA (eds) Insect plant interactions and induced plant defense. Wiley, West Sussex, pp 132–146

    Chapter  Google Scholar 

  • Bois E, Lieutier F (1997) Phenolic response of Scots pine clones to inoculation with Leptographium wingfieldii, a fungus associated with Tomicus piniperda. Plant Physiol Biochem 35:819–825

    CAS  Google Scholar 

  • Bonello P, Blodgett JT (2003) Pinus nigra–Sphaeropsis sapinea as a model pathosystem to investigate local and systemic effects of fungal infection of pines. Physiol Mol Plant Pathol 63:249–261

    Article  Google Scholar 

  • Bonello P, Gordon TR, Storer AJ (2001) Systemic induced resistance in Monterey pine. For Pathol 31:99–106

    Google Scholar 

  • Brignolas F, Lacroix B, Lieutier F, Sauvard D, Drouet A, Claudot A-C, Yart A, Berryman AA, Christiansen E (1995) Induced responses in phenolic metabolism in two Norway spruce clones after wounding and inoculation with Ophiostoma polonicum a bark beetle-associated fungus. Plant Physiol 109:821–827

    PubMed  CAS  Google Scholar 

  • Byun-McKay SA, Hunter WL, Godard K-A, Wang SW, Martin DM, Bohlmann J, Plant AL (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (−)-pinene synthase in Sitka spruce. Plant Physiol 133:368–378

    Article  CAS  Google Scholar 

  • Christiansen E, Krokene P, Berryman AA, Franceschi VR, Krekling T, Lieutier F, Lönneborg A, Solheim H (1999) Mechanical injury and fungal infection induce acquired resistance in Norway spruce. Tree Physiol 19:399–403

    PubMed  Google Scholar 

  • Chung MC, Chou SJ, Kuang LY, Chang YY, Yang SF (2002) Subcellular localization of 1-aminocyclopropane-1-carboxylic acid oxidase in apple fruit. Plant Cell Physiol 43:549–554

    Article  PubMed  CAS  Google Scholar 

  • Dong JG, Fernandez-Maculet JC, Yang SF (1992) Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc Natl Acad Sci USA 89:9789–9793

    Article  PubMed  CAS  Google Scholar 

  • Eklund L, Little CHA (1998) Ethylene evolution, radial growth and carbohydrate concentrations in Abies balsamea shoots ringed with ethrel. Tree Physiol 18:383–391

    PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Fäldt J, Martin D, Miller B, Rawat S, Bohlmann J (2003) Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol Biol 51:119–133

    Article  PubMed  Google Scholar 

  • Felsenstein J (1993) PHYLIP (phylogeny inference package) version 3.62. Distributed by the author. Department of Genetics, University of Washington, Seattle

  • Franceschi VR, Krekling T, Berryman AA, Christiansen E (1998) Specialized phloem parenchyma cells in Norway spruce (Pinaceae) bark are an important site of defense reactions. Am J Bot 85:601–615

    Article  Google Scholar 

  • Franceschi VR, Krokene P, Krekling T, Berryman AA, Christiansen E (2000) Phloem parenchyma cells are involved in local and distant defense responses to fungal inoculation or bark-beetle attack in Norway spruce (Pinaceae). Am J Bot 87:314–326

    Article  PubMed  Google Scholar 

  • Franceschi VR, Krekling T, Christiansen E (2002) Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am J Bot 89:578–586

    Article  CAS  Google Scholar 

  • Franceschi VR, Krokene P, Christiansen E, Krekling T (2005) Tansley review: anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:353–376

    Article  PubMed  CAS  Google Scholar 

  • Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685–695

    PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed  CAS  Google Scholar 

  • Huber DPW, Ralph S, Bohlmann J (2004) Genomic hardwiring and phenotypic plasticity of terpenoid-based defenses in conifers. J Chem Ecol 30:2399–2418

    Article  PubMed  CAS  Google Scholar 

  • Huber DPW, Philippe RN, Madilao L, Sturrock RN, Bohlmann J (2005) Changes in anatomy and terpene chemistry in roots of Douglas-fir seedlings following treatment with methyl jasmonate. Tree Physiol 25:1075–1083

    PubMed  CAS  Google Scholar 

  • Hudgins JW, Franceschi VR (2004) Methyl jasmonate-induced ethylene production is responsible for phloem defense responses and reprogramming of conifer stem cambial zone for traumatic resin duct formation. Plant Physiol 135:2134–2149

    Article  PubMed  CAS  Google Scholar 

  • Hudgins JW, Christiansen E, Franceschi VR (2003a) Methyl jasmonate induces changes mimicking anatomical defenses in diverse members of the Pinaceae. Tree Physiol 23:361–371

    CAS  Google Scholar 

  • Hudgins JW, Krekling T, Franceschi VR (2003b) Distribution of calcium oxalate crystals in the secondary phloem of conifers: a constitutive defense mechanism? New Phytol 159:677–690

    Article  CAS  Google Scholar 

  • Hudgins JW, Christiansen E, Franceschi VR (2004) Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic treatment. Tree Physiol 24:251–264

    PubMed  CAS  Google Scholar 

  • Ingemarsson BS, Lundqvist ME, Eliasson L (1991) Seasonal variation in ethylene concentration in the wood of Pinus sylvestris L. Tree Physiol 8:273–279

    PubMed  CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    PubMed  CAS  Google Scholar 

  • Katoh S, Croteau R (1997) Individual variation in constitutive and induced monoterpene biosynthesis in grand fir. Phytochemistry 47:577–582

    Article  Google Scholar 

  • Keeling CI, Bohlmann J (2006) Genes, enzymes, and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol (in press)

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

    Article  CAS  Google Scholar 

  • Kim YS, Yang SF (1994) Structure and expression of cDNAs encoding 1-aminocyclopropane-1-carboxylate oxidase homologs isolated from excised mung bean hypocotyls. Planta 194:223–229

    Article  PubMed  CAS  Google Scholar 

  • Kim YS, Choi D, Lee MM, Lee SH, Kim WT (1998) Biotic and abiotic stress-related expression of 1-aminocyclopropane-1-carboxylate oxidase gene family in Nicotiana glutinosa L. Plant Cell Physiol 39:565–573

    PubMed  CAS  Google Scholar 

  • Klintborg A, Eklund L, Little CHA (2002) Ethylene metabolism in Scots pine (Pinus sylvestris) shoots during the year. Tree Physiol 22:59–66

    PubMed  CAS  Google Scholar 

  • Kolosova N, Miller B, Ralph S, Ellis BE, Douglas C, Ritland K, Bohlmann J (2004) Isolation of high-quality RNA from gymnosperm and angiosperm trees. Biotechniques 36:821–824

    PubMed  CAS  Google Scholar 

  • Krekling T, Franceschi VR, Berryman AA, Christiansen E (2000) The structure and development of polyphenolic parenchyma cells in Norway spruce (Picea abies) bark. Flora 195:354–369

    Google Scholar 

  • Krokene P, Christiansen E, Solheim H, Berryman AA, Franceschi VR (1999) Induced resistance to pathogenic fungi in Norway spruce. Plant Physiol 121:565–570

    Article  PubMed  CAS  Google Scholar 

  • Krokene P, Solheim H, Krekling T, Christiansen E (2003) Inducible anatomical defense responses in Norway spruce stems and their possible role in induced resistance. Tree Physiol 23:191–197

    PubMed  Google Scholar 

  • Kusumoto D, Suzuki K (2003) Spatial distribution and time-course of polyphenol accumulation as a defense response induced by wounding in the phloem of Chamaecyparis obtuse. New Phytol 10:1469–1481

    Google Scholar 

  • Langenheim JH (2003) Plant resins: chemistry, evolution, ecology, and ethnobotany. Timber Press, Portland

    Google Scholar 

  • Lay VJ, Prescott AG, Thomas PG, John P (1996) Heterologous expression and site-directed mutagenesis of the 1-aminocyclopropane-1-carboxylate oxidase from kiwi fruit. Eur J Biochem 242:228–234

    Article  PubMed  CAS  Google Scholar 

  • Lev-Yadun S, Aloni R (1995) Differentiation of the ray system in woody-plants. Bot Rev 61:45–84

    Google Scholar 

  • Lieutier F, Sauvard D, Brignolas F, Picron V, Yart A, Bastien C, Jay-Allemand C (1996) Changes in phenolic metabolites of Scots pine phloem induced by Ophiostoma brunneo-cilatum, a bark beetle-associated fungus. Eur J For Pathol 26:145–158

    Article  Google Scholar 

  • Little CHA, Eklund L (1999) Ethylene in relation to compression wood formation in Abies balsamea shoots. Trees 13:173–177

    Google Scholar 

  • Martin D, Bohlmann J (2005) Molecular biochemistry and genomics of terpenoid defenses in conifers. Rec Adv Phytochem 39:29–56

    CAS  Google Scholar 

  • Martin D, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018

    Article  PubMed  CAS  Google Scholar 

  • Martin DM, Fäldt J, Bohlmann J (2004) Functional characterization of nine Norway spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol 135:1908–1927

    Article  PubMed  CAS  Google Scholar 

  • Miller B, Madilao L, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137:369–382

    Article  PubMed  CAS  Google Scholar 

  • Nagy NE, Franceschi VR, Solheim H, Krekling T, Christiansen E (2000) Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am J Bot 87:302–313

    Article  PubMed  Google Scholar 

  • Nagy NE, Fossdal CG, Krokene P, Krekling T, Lønneborg A, Solheim H (2004) Induced responses to pathogen infection in Norway spruce phloem: changes in polyphenolic parenchyma cells, chalcone synthase transcript levels and peroxidase activity. Tree Physiol 24:505–515

    PubMed  CAS  Google Scholar 

  • Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–36

    Article  PubMed  CAS  Google Scholar 

  • Page RD (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Pan HF, Lundgren LN (1996) Phenolics from inner bark of Pinus sylvestris. Phytochemistry 42:1185–1189

    Article  CAS  Google Scholar 

  • Phillips MA, Croteau R (1999) Resin-based defenses in conifers. Trends Plant Sci 5:184–190

    Article  Google Scholar 

  • Plomion C, Pionneau C, Brach J, Costa P, Bailleres H (2000) Compression wood-responsive proteins in developing xylem of maritime pine (Pinus pinaster Ait.). Plant Physiol 123:959–969

    Article  PubMed  CAS  Google Scholar 

  • Popp M, Johnson JD, Lesney M (1995) Changes in ethylene production and monoterpene concentration in slash pine and loblolly pine following inoculation with bark beetle vectored fungi. Tree Physiol 15:807–812

    CAS  Google Scholar 

  • Prescott AG, John P (1996) Dioxygenases: molecular structure and role in plant metabolism. Annu Rev Plant Physiol Plant Mol Biol 47:245–271

    Article  PubMed  CAS  Google Scholar 

  • Raffa KF, Aukema BH, Erbilgin N, Klepzig KD, Wallin KF (2005) Interactions among conifer terpenoids and bark beetles across multiple levels of scale: an attempt to understand population patterns and physiological processes. Rec Adv Phytochem 39:79–118

    CAS  Google Scholar 

  • Ralph S, Park JY, Bohlmann J, Mansfield SD (2006a) Dirigent proteins in insect-induced conifer defense: discovery, phylogeny and differential expression of a family of DIR and DIR-like genes in spruce. Plant Mol Biol 60:21–40

    Article  CAS  Google Scholar 

  • Ralph S, Yueh H, Friedmann MF, Aeschliman D, Zeznik JA, Nelson CC, Butterfield YSN, Kirkpatrick R, Liu J, Jones SJM, Marra MA, Douglas CJ, Ritland K, Bohlmann J (2006b) Conifer defense against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworm (Choristoneura occidentalis) or white pine weevil (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ (in press)

  • Ramassamy S, Olmos E, Bouzayen M, Pech JC, Latche A (1998) 1-Aminocyclopropane-1-carboxylate oxidase of apple fruit is periplasmic. J Exp Bot 49:1909–1915

    Article  CAS  Google Scholar 

  • Reinhardt D, Kende H, Boller T (1994) Subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in tomato cells. Planta 195:142–146

    Article  CAS  Google Scholar 

  • Reynolds EA, John P (2000) ACC oxidase is found in seedlings of two (Coniferales, Gnetales) of the four gymnosperm orders. Physiol Plant 110:38–41

    Article  CAS  Google Scholar 

  • Roach PL, Clifton IJ, Fueloep V, Harlos K, Barton GJ, Hajdu J, Andersson I, Schofield CJ, Baldwin JE (1995) Crystal structure of isopenicillin-n-synthase is the first from a new structural family of enzymes. Nature 375:700–704

    Article  PubMed  CAS  Google Scholar 

  • Rocklin AM, Tierney DL, KofmanV, Brunhuber NMW, Hoffman BM, Christoffersen RE, Reich NO, Lipscomb JD, Que L Jr (1999) Role of the nonheme Fe (II) center in the biosynthesis of the plant hormone ethylene. Proc Natl Acad Sci USA 96:7905–7909

    Article  PubMed  CAS  Google Scholar 

  • Rombaldi C, Lelievre JM, Latche A, Petitprez M, Bouzayen M, Pech JC (1994) Immunocytolocalization of 1-aminocyclopropane-1-carboxylic acid oxidase in tomato and apple fruit. Planta 192:453–460

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Zeneli G, Hietala AM, Fossdal CG, Krokene P, Christiansen E, Gershenzon J (2005) Induced chemical defenses in conifers. Rec Adv Phytochem 39:1–28

    CAS  Google Scholar 

  • Seo YS, Yoo A, Jung J, Sung S-K, Yang DR, Kim WT, Lee W (2004) The active site and substrate-binding mode of 1-aminocyclopropane-1-carboxylate oxidase determined by site-directed mutagenesis and comparative modeling studies. Biochem J 38:339–346

    Article  Google Scholar 

  • Seybold SJ, Bohlmann J, Raffa KF (2000) Biosynthesis of coniferophagous bark beetle pheromones and conifer isoprenoids: evolutionary perspective and synthesis. Can J Entomol 132:697–753

    Article  Google Scholar 

  • Telewski FW, Wakefield AH, Jaffe MJ (1983) Computer-assisted image analysis of tissues of ethrel-treated Pinus taeda seedlings. Plant Physiol 72:177–181

    Article  PubMed  CAS  Google Scholar 

  • Tierney DL, Rocklin AM, Lipscomb JD, Que L Jr, Hoffman BM (2005) ENDOR studies of the ligation and structure of the non-heme iron site in ACC oxidase. J Am Chem Soc 127:7005–7013

    Article  PubMed  CAS  Google Scholar 

  • Tomlin ES, Alfaro RI, Borden JH, He F (1998) Histological response of resistant and susceptible white spruce to simulated white pine weevil damage. Tree Physiol 18:21–28

    PubMed  Google Scholar 

  • Trapp S, Croteau R (2001) Defensive resin biosynthesis in conifers. Annu Rev Plant Physiol Plant Mol Biol 52:689–724

    Article  PubMed  CAS  Google Scholar 

  • Viiri H, Annila E, Kitunen V, Niemelia P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15:112–122

    Article  CAS  Google Scholar 

  • Yamamoto F, Kozlowski TT (1987) Effects of flooding, tilting of stems, and ethrel application on growth, stem anatomy and ethylene production of Pinus densiflora seedlings. J Exp Bot 38:293–310

    Article  CAS  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Zhang Z, Ren J-S, Clifton IJ, Schofield CJ (2004) Crystal structure and mechanistic implications of 1-aminocyclopropane-1-carboxylic acid oxidase-the ethylene forming enzyme. Chem Biol 11:1383–1394

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Rocklin AM, Lipscomb JD, Que L Jr, Solomon EI (2002) Spectroscopic studies of 1-aminocyclopropane-1-carboxylic acid oxidase: molecular mechanism and CO2 activation in the biosynthesis of ethylene. J Am Chem Soc 124:4602–4609

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Confocal and TEM microscopy was done in the Electron Microscopy Center, Washington State University. We thank Sharon Jancsik for technical assistance with cDNA cloning and RNA isolation. This work was generously supported by grants to JB from Genome Canada, Genome British Columbia, and the province of British Columbia; the Natural Sciences and Engineering Research Council of Canada (NSERC); and with infrastructure funds from the Canadian Foundation for Innovation (CFI) and the British Columbia Knowledge and Development Funds (BCKDF). This paper is dedicated in memory of Dr. Vincent R. Franceschi (1953–2005). Vince was a leading scientist who contributed greatly to plant sciences through his teaching, research, generous collaborative support, and countless other activities. His work on the cell biology of conifer defense has been a great inspiration and provided an important foundation for many current and future studies.

Author information

Authors and Affiliations

  1. Michael Smith Laboratories, University of British Columbia, 321-2185 East Mall, Vancouver, BC, Canada, V6T 1Z4

    J. W. Hudgins, Steven G. Ralph & Jörg Bohlmann

  2. Department of Botany, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4

    Jörg Bohlmann

  3. Department of Forest Sciences, University of British Columbia, Vancouver, BC, Canada, V6T 1Z4

    Jörg Bohlmann

  4. School of Biological Sciences, Washington State University, Pullman, WA, 99164-4236, USA

    J. W. Hudgins & Vincent R. Franceschi

Authors
  1. J. W. Hudgins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Steven G. Ralph
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vincent R. Franceschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jörg Bohlmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jörg Bohlmann.

Additional information

J.W. Hudgins and Steven G. Ralph contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hudgins, J.W., Ralph, S.G., Franceschi, V.R. et al. Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells. Planta 224, 865–877 (2006). https://doi.org/10.1007/s00425-006-0274-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0274-4

Keywords

Search

Navigation