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Differential responses of the promoters from nearly identical paralogs of loblolly pine (Pinus taeda L.) ACC oxidase to biotic and abiotic stresses in transgenic Arabidopsis thaliana

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Abstract

Promoters from an ACC oxidase gene (PtACO1) and its nearly identical paralog (NIP) (PtACO2) of loblolly pine (Pinus taeda L.) were recovered from genomic DNA using PCR amplification. Transgenic Arabidopsis plants harboring genetic constructs from which β-glucuronidase (GUS) expression was driven by the full-length (pACO1:GUS, pACO2:GUS) or truncated (pACO1-1.2:GUS, pACO2-1.2:GUS) loblolly pine ACC oxidase gene promoters displayed distinctive patterns of expression for the different promoter constructs. Both full-length promoter constructs, but not those using truncated promoters, responded to indole-3-acetic acid (IAA) and wounding. Both pACO1:GUS and pACO1-1.2:GUS responded to pathogen attack, while neither version of the pACO2 promoter responded to infection. In the inflorescence stalks, the full-length pACO1 promoter construct, but not the truncated pACO1-1.2:GUS or either pACO2 construct, responded to bending stress. When flowering transgenic Arabidopsis plants were placed in a horizontal position for 48 h, expression from pACO2:GUS, but not the other constructs, was induced on the underside of shoots undergoing gravitropic reorientation. The expression pattern for the pACO2:GUS construct in transgenic Arabidopsis was consistent with what might be expected for a gene promoter involved in the compression wood response in loblolly pine. Although near complete sequence identity between PtACO1 and PtACO2 transcripts prevented quantitation of specific gene products, the promoter expression analyses presented in this study provide strong evidence that the two ACC oxidase genes are likely differentially expressed and responded to different external stimuli in pine. These results are discussed with respect to the potential functional differences between these two genes in loblolly pine.

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Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylate

CaMV:

Cauliflower mosaic virus

GUS:

Glucuronidase

IAA:

Indole acetic acid

PGRs:

Plant growth regulators

X-gluc:

5-Bromo-4-chloro-3-indolyl-β-d-glucuronide

References

  1. Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology. Academic Press, San Diego, pp 108–113

  2. Aloni R (2001) Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J Plant Growth Regul 20:22–34

  3. Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–853

  4. 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

  5. Atkinson RG, Bolitho KM, Wright MA, Iturriagagoitia-Bueno T, Reid SJ, Ross GS (1998) Apple ACC-oxidase and polygalacturonase: ripening-specific gene expression and promoter analysis in transgenic tomato. Plant Mol Biol 38:449–460

  6. Avila C, Cantón FR, Barnestein P, Suárez M-F, Marraccini P, Rey M, Humara JM, Ordás R, Cánovas FM (2001) The promoter of a cytosolic glutamine synthetase gene from the conifer Pinus sylvestris is active in cotyledons of germinating seeds and light-regulated in transgenic Arabidopsis thaliana. Physiol Plant 112:388–396

  7. Barnes JR, Lorenz WW, Dean JFD (2008) Characterization of a 1-aminocyclopropane-1-carboxylate synthase gene from loblolly pine (Pinus taeda L.). Gene 413:18–31

  8. Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9:525–535

  9. Blake TJ, Pharis RP, Reid DM (1980) Ethylene, gibberellins, auxin and the apical control of branch angle in a conifer, Cupressus arizonica. Planta 148:64–68

  10. Blume B, Grierson D (1997) Expression of ACC oxidase promoter–GUS fusions in tomato and Nicotiana plumbaginifolia regulated by developmental and environmental stimuli. Plant J 12:731–746

  11. Chae HS, Kieber JJ (2005) Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci 10:291–296

  12. Chae HS, Cho YG, Park MY, Lee MC, Eun MY, Kang BG, Kim WT (2000) Hormonal cross-talk between auxin and ethylene differentially regulates the expression of two members of the 1-aminocyclopropane-1-carboxylate oxidase gene family in rice (Oryza sativa L.). Plant Cell Physiol 41:354–362

  13. Chen BC-M, McManus MT (2006) Expression of 1-aminocyclopropane-1-carboxylate (ACC) oxidase genes during the development of vegetative tissues in white clover (Trifolium repens L.) is regulated by ontological cues. Plant Mol Biol 60:451–467

  14. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

  15. Core HA, Côté WA, Day AC (1976) Wood structure and identification. Syracuse University Press, Syracuse, pp 37–40

  16. Du S, Sugano M, Tsushima M, Nakamura T, Yamamoto F (2004) Endogenous indole-3-acetic acid and ethylene evolution in tilted Metasequoia glyptostroboides stems in relation to compression-wood formation. J Plant Res 117:171–174

  17. Emrich SJ, Li L, Wen TJ, Yandeau-Nelson MD, Fu Y, Guo L, Chou HH, Aluru S, Ashlock DA, Schnable PS (2007) Nearly identical paralogs: implications for maize (Zea mays L.) genome evolution. Genetics 175:429–439

  18. Englert C, Hou X, Maheswaran S, Bennett P, Ngwu C, Re GG, Garvin AJ, Rosner MR, Haber DA (1995) WT1 suppresses synthesis of the epidermal growth factor receptor and induces apoptosis. EMBO J 14:4662–4675

  19. Funada R, Mizukami E, Kubo T, Fushitani M, Sugiyama T (1990) Distribution of indole-3-acetic acid and compression wood formation in the stems of inclined Cryptomerica japonica. Holzforschung 44:331–334

  20. Godard K-A, Byun-McKay A, Levasseur C, Plant A, Séguin A, Bohlmann J (2007) Testing of a heterologous, wound- and insect-inducible promoter for functional genomics studies in conifer defense. Plant Cell Rep 26:2083–2090

  21. Gould JH, Zhou Y, Padmanabhan V, Magallanes-Cedeno ME, Newton RJ (2002) Transformation and regeneration of loblolly pine: shoot apex inoculation with Agrobacterium. Mol Breeding 10:131–141

  22. Hamilton AJ, Bouzayen M, Grierson D (1991) Identification of a tomato gene for the ethylene-forming enzyme by expression in yeast. Proc Natl Acad Sci USA 88:7434–7437

  23. Hellgren JM, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 135:212–220

  24. Henskens JAM, Rouwendal GJA, Ten Have A, Woltering EJ (1994) Molecular cloning of two different ACC synthase PCR fragments in carnation flowers and organ-specific expression of the corresponding genes. Plant Mol Biol 26:453–458

  25. Höfig KP, Moyle RL, Putterill J, Walter C (2003) Expression analysis of four Pinus radiata male cone promoters in the heterologous host Arabidopsis. Planta 217:858–867

  26. Holdsworth MJ, Bird CR, Ray J, Schuch W, Grierson D (1987) Structure and expression of an ethylene-related mRNA from tomato. Nucl Acid Res 15:731–739

  27. Hudgins JW, Ralph SG, Franceschi VR, Bohlmann J (2006) Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-carboxylic acid oxidase in resin duct and phenolic parenchyma cells. Planta 224:865–877

  28. Itai A, Kawata T, Tanabe K, Tamura F, Uchiyama M, Tomomitsu M, Shiraiwa N (1999) Identification of 1-aminocyclopropane-1-carboxylic acid synthase genes controlling the ethylene level of ripening fruit in Japanese pear (Pyrus pyrifolia Nakai). Mol Gen Genet 261:42–49

  29. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

  30. Kim WT, 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

  31. 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

  32. Kimbrough JM, Salinas-Mondragon S, Boss WF, Brown CS, Sederoff HW (2004) The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 136:790–2805

  33. Kwon M, Bedgar DL, Piastuch W, Davin LB, Lewis NG (2001) Induced compression wood formation in Douglas fir (Pseudotsuga menziesii) in microgravity. Phytochemistry 57:847–857

  34. Lasserre E, Bouqin T, Hernandez JA, Bull J, Pech JC, Balague C, Bull J (1996) Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.). Mol Gen Genet 251:81–90

  35. Lasserre R, Godard F, Bouqin T, Hernandez JA, Pech JC, Roby D, Balague C (1997) Differential activation of two ACC oxidase gene promoters from melon during plant development and in response to pathogen attack. Mol Gen Genet 256:211–222

  36. 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

  37. Lazo GR, Stein PA, Ludwig RA (1991) DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Nat Biotechnol 9:963–967

  38. Le Provost G, Paiva J, Pot D, Brach J, Plomion C (2003) Seasonal variation in transcript accumulation in wood-forming tissues of maritime pine (Pinus pinaster Ait.) with emphasis on a cell wall glycine-rich protein. Planta 217:820–830

  39. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl Acids Res 30:325–327

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

  41. Little CHA, Lavigne MB (2002) Gravimorphism in current-year shoots of Abies balsamea: involvement of compensatory growth, indole-3-acetic acid transport and compression wood formation. Tree Physiol 22:311–320

  42. Liu X, Shiomi S, Nakatsuka A, Kubo Y, Nakamura R, Inaba A (1999) Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiol 121:1257–1265

  43. Liu JJ, Ekramoddoullah AKM, Piggott N, Zamani A (2005) Molecular cloning of a pathogen/wound-inducible PR10 promoter from Pinus monticola and characterization in transgenic Arabidopsis plants. Planta 221:159–169

  44. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272

  45. López-Gómez R, Morales-Domínguez F, Mendoza Alcázar O, Gómez-Lim MA (2004) Identification of a genomic clone to ACC oxidase from papaya (Carica papaya L.) and expression studies. J Agric Food Chem 52:794–800

  46. Mita S, Kawamura S, Yamawaki K, Nakamura K, Hyodo H (1998) Differential expression of genes involved in the biosynthesis and perception of ethylene during ripening of passion fruit (Passiflora edulis Sims). Plant Cell Physiol 39:1209–1217

  47. Moon H, Callahan AM (2004) Developmental regulation of peach ACC oxidase promoter-GUS fusions in transgenic tomato fruits. J Exp Bot 55:1519–1528

  48. Morgan PW, Drew MC (1997) Ethylene and plant response to stress. Physiol Plant 100:620–630

  49. Morita MT, Tasaka T (2004) Gravity sensing and signaling. Curr Opin Plant Biol 7:712–718

  50. Nadeau JA, Zhang XS, Nair H, O’Neill SD (1993) Temporal and spatial regulation of 1-aminocyclopropane-1-carbocylate oxidase in the pollination-induced senescence of orchid flowers. Plant Physiol 103:31–39

  51. Nakatsuka A, Shiomi S, Kubo Y, Inaba A (1997) Expression and internal feedback regulation of ACC synthase and ACC oxidase genes in ripening tomato fruit. Plant Cell Physiol 38:1103–1110

  52. Nie X, Singh RP, Tai GCC (2002) Molecular characterization and expression analysis of 1-aminocyclopropane-1-carboxylate oxidase homologs from potato under abiotic and biotic stresses. Genome 45:913–950

  53. Pastuglia M, Roby D, Dumas C, Cock JM (1997) Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase in Brassica oleracea. Plant Cell 9:49–60

  54. Plomion C, Pionneau C, Brach J, Costa P, Baillerès H (2000) Compression wood-responsive proteins in developing xylem of maritime pine (Pinus pinaster Ait.). Plant Physiol 123:959–970

  55. Raz V, Ecker JR (1999) Regulation of differential growth in the apical hook of Arabidopsis. Development 126:3661–3668

  56. Rodrigues-Pousada RA, De Rycke R, Dedonder A, Van Caeneghem W, Engler G, Van Montagu M, Van Der Straeten D (1993) The Arabidopsis 1-Aminocyclopropane-1-carboxylate synthase gene 1 is expressed during early development. Plant Cell 5:897–911

  57. Ross GS, Knighton ML, Lay-Yee M (1992) An ethylene-related cDNA from ripening apples. Plant Mol Biol 19:231–238

  58. Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523

  59. Ruperti B, Bonghi C, Rasori A, Ramina A, Tonutti P (2001) Characterization and expression of two members of the peach 1-aminocyclopropane-1-carboxylate oxidase gene family. Physiol Plant 111:336–344

  60. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700

  61. Salman-Minkov A, Levi A, Wolf S, Trebitsh T (2008) ACC synthase genes are polymorphic in watermelon (Citrullus spp.) and differentially expressed in flowers and in response to auxin and gibberellin. Plant Cell Physiol 49:740–750

  62. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring harbor Laboratory Press, Cold Spring Harbor, pp 93–94

  63. Savidge RA (1983) The role of plant hormones in higher plant cellular differentiation. II. Experiments with the vascular cambium, and sclereid and tracheid differentiation in the pine, Pinus contorta. Histochem J 15:447–466

  64. Solano R, Nieto C, Avila J, Cañas L, Diaz I, Paz-Ares J (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 14:1773–1784

  65. Spanu P, Reinhardt D, Boller T (1991) Analysis and cloning of the ethylene-forming enzyme from tomato by functional expression of its messenger-RNA in Xenopus-laevis oocytes. EMBO J 10:2007–2013

  66. Sundberg B, Little CHA (1990) Tracheid production in response to changes in the internal level of indole-3-acetic acid in 1-year-old shoots of Scott pine. Plant Physiol 94:1721–1727

  67. Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signaling pathways to control plant development. Plant Mol Biol 49:409–424

  68. Tang X, Wang H, Brandt AS, Woodson WR (1993) Organization and structure of the 1-aminocyclopropane-1-carboxylate oxidase gene family from Petunia hybrida. Plant Mol Biol 23:1151–1164

  69. Tang W, Sederoff R, Whetten R (2001) Regeneration of transgenic loblolly pine (Pinus taeda L.) from zygotic embryos transformed with Agrobacterium tumefaciens. Planta 213:981–989

  70. Telewski FW (1990) Growth, wood density, and ethylene production in response to mechanical perturbation in Pinus taeda. Can J For Res 20:1277–1282

  71. Timell TE (1986) Compression wood in gymnosperms. Springer, Heidelberg, vol 2, pp 733, 983–1262

  72. 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

  73. Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5:1529–1539

  74. Wang NN, Shih MC, Li N (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56:909–920

  75. Weterings K, Pezzotti M, Cornelissen M, Mariani C (2002) Dynamic 1-aminocyclopropane-1-carboxylate-synthase and–oxidase transcript accumulation patterns during pollen tube growth in tobacco styles. Plant Physiol 130:1190–1200

  76. White AJ, Dunn MA, Brown K, Hughes MA (1994) Comparative analysis of genomic sequence and expression of a lipid transfer protein gene family in winter barley. J Exp Bot 45:1885–1892

  77. Wilson BF, Chien CT, Zaerr JB (1989) Distribution of endogenous indole-3-acetic acid and compression wood formation in reoriented branches of Douglas-fir. Plant Physiol 91:338–344

  78. Woeste KE, Vogel JP, Kieber JJ (1999) Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol Plant 105:478–484

  79. Yamaguchi-Shinozaki K, Shinozaki K (1993) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120

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

  81. Yu SJ, Kim S, Lee JS, Lee DH (1998) Differential accumulation of transcripts for ACC synthase and ACC oxidase homologs in etiolated mung bean hypocotyls in response to various stimuli. Mol Cells 8:350–358

  82. Yuan S, Wang Y, Dean JFD (2010) ACC oxidase genes expressed in the wood-forming tissues of loblolly pine (Pinus taeda L.) include a pair of Nearly Identical Paralogs (NIPs). Gene 453:24–36

  83. Zhang Y, Sederoff RR, Allona I (2000) Differential expression of genes encoding cell wall proteins in vascular tissues from vertical and bent loblolly pine trees. Tree Physiol 20:457–466

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Acknowledgments

We thank Dr. C. J. Nairn for providing plant materials, vectors and numerous technical suggestions. Thanks also to Dr. S.A. Merkle for assistance with photomicrographs. This work was funded by United States Department of Agriculture (grant number 98-35103-6534) to J.F.D.D.

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Correspondence to Jeffrey F. D. Dean.

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Yuan, S., Dean, J.F.D. Differential responses of the promoters from nearly identical paralogs of loblolly pine (Pinus taeda L.) ACC oxidase to biotic and abiotic stresses in transgenic Arabidopsis thaliana . Planta 232, 873–886 (2010). https://doi.org/10.1007/s00425-010-1224-8

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Keywords

  • Auxin
  • Bending stress
  • Compression wood
  • Conifer
  • Ethylene biosynthesis
  • Nearly identical paralogs (NIPs)