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Repression of gibberellin biosynthesis or signaling produces striking alterations in poplar growth, morphology, and flowering

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Abstract

We modified gibberellin (GA) metabolism and signaling in transgenic poplars using dominant transgenes and studied their effects for 3 years under field conditions. The transgenes that we employed either reduced the bioactive GAs, or attenuated their signaling. The majority of transgenic trees had significant and in many cases dramatic changes in height, crown architecture, foliage morphology, flowering onset, floral structure, and vegetative phenology. Most transgenes elicited various levels of height reduction consistent with the roles of GA in elongation growth. Several other growth traits were proportionally reduced, including branch length, internode distance, and leaf length. In contrast to elongation growth, stem diameter growth was much less affected, suggesting that semi-dwarf trees in dense stands might provide high levels of biomass production and carbon sequestration. The severity of phenotypic effects was strongly correlated with transgene expression among independent transgenic events, but often in a non-linear manner, the form of which varied widely among constructs. The majority of semi-dwarfed, transgenic plants showed delayed bud flush and early bud set, and expression of a native GAI transgene accelerated first time flowering in the field. All of the phenotypic changes observed in multiple years were stable over the 3 years of field study. Our results suggest that transgenic modification of GA action may be useful for producing semi-dwarf trees with modified growth and morphology for horticulture and other uses.

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Abbreviations

GA:

Gibberellins

GA2ox:

Gibberellin 2 oxidase

GAI:

GA insensitive

RGL:

Repressor of GA1 like

References

  1. Atkinson C, Else M (2001) Understanding how rootstocks dwarf fruit trees. Compact Fruit Tree 34:46–49

  2. Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265

  3. Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

  4. Bradshaw HD, Strauss SH (2001) Breeding strategies for the 21st century: Domestication of poplar. In: Dickman DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. Part B. NRC Research Press, Ottawa, pp 383–394

  5. Brunner AM, Nilsson O (2004) Revisiting tree maturation and floral initiation in the poplar functional genomics era. New Phytol 164:43–51

  6. Brunner AM, Li JY, DiFazio SP, Shevchenko O, Montgomery BE, Mohamed R, Wei H, Ma C, Elias AA, VanWormer K, Strauss SH (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100

  7. Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291

  8. Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299

  9. Chandler PM, Robertson M (1999) Gibberellin dose-response curves and the characterization of dwarf mutants of barley. Plant Physiol 120:623–632

  10. Curtis IS, Hanada A, Yamaguchi S, Kamiya Y (2005) Modification of plant architecture through the expression of GA 2-oxidase under the control of an estrogen inducible promoter in Arabidopsis thaliana L. Planta 222:957–967

  11. David CC, Otsuka K (1994) Modern rice technology and income distribution in Asia. Lynne Reinner, Boulder, pp 3–17

  12. Davies PJ (1995) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer, London, pp 6–7

  13. Dijkstra C, Adams E, Bhattacharya A, Page AF, Anthony P, Kourmpetli S, Power JB, Lowe KC, Thomas SG, Hedden P, Phillips AL, Davey MR (2008) Over-expression of a gibberellin 2-oxidase gene from Phaseolus coccineus L. enhances gibberellin inactivation and induces dwarfism in Solanum species. Plant Cell Rep 27:463–470

  14. Eriksson ME, Moritz T (2002) Daylength and spatial expression of a gibberellin 20-oxidase isolated from hybrid aspen (Populus tremula L. × P. tremuloides Michx.). Planta 214:920–930

  15. Filichkin SA, Meilan R, Busov VB, Ma C, Brunner AM, Strauss SH (2006) Alcohol-inducible gene expression in transgenic Populus. Plant Cell Rep 25:660–667

  16. Fu X, Sundhakar D, Peng J, Richards DE, Christou P, Harberd NP (2001) Expression of Arabidopsis GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13:1791–1802

  17. Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in populus through interactions with auxin and other hormones. Plant Cell 22:623–639

  18. Gressel J (1999) Tandem constructs: preventing the rise of superweeds. Trends Biotechnol 17:361–366

  19. Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: How an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21:1328–1339

  20. Hedden P, Phillips AL, Rojas MC, Carrera E, Tudzynski B (2001) Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? J Plant Growth Regul 20:319–331

  21. Hynes LW, Peng J, Richards DE, Harberd NP (2003) Transgenic expression of the Arabidopsis DELLA proteins GAI and gai confers altered gibberellin response in tobacco. Transgenic Res 12:707–714

  22. Itoh H, Ueguchi-Tanaka M, Matsuoka M (2008) Molecular biology of gibberellins signaling in higher plants. Int Rev Cell Mol Biol 268:191–221

  23. Jackson DA (1993) Stopping rules in principle components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214

  24. Lee DJ, Zeevaart JA (2005) Molecular cloning of GA 2-oxidase3 from spinach and its ectopic expression in Nicotiana sylvestris. Plant Physiol 138:243–254

  25. Leple JC, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, Naumann A, Kang KY, Kim H, Ruel K, Lefebvre A, Joseleau JP, Grima-Pettenati J, De Rycke R, Andersson-Gunneras S, Erban A, Fehrle I, Petit-Conil M, Kopka J, Polle A, Messens E, Sundberg B, Mansfield SD, Ralph J, Pilate G, Boerjan W (2007) Downregulation of cinnamoyl-coenzyme a reductase in poplar: Multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19:3669–3691

  26. Li JY, Brunner AM, Meilan R, Strauss SH (2009) Stability of transgenes in trees: expression of two reporter genes in poplar over three field seasons. Tree Physiol 29:299–312

  27. Lo SF, Yang SY, Chen KT, Hsing YL, Zeevaart JAD, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603–2618

  28. Milliken GA, Johnson DE (1984) Analysis of messy data. Van Nostrand Reinhold, New York

  29. Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688

  30. Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989

  31. Nagano H, Onishi K, Ogasawara M, Horiuchi Y, Sano Y (2005) Genealogy of the “Green Revolution” gene in rice. Genes Genet Syst 80:351–356

  32. Olsen JE (2010) Light and temperature sensing and signaling in induction of bud dormancy in woody plants. Plant Mol Biol 73:37–47

  33. Olsen JE, Juntilla O, Moritz T (1995) A localized decrease of GA1 in shoot tips of Salix pentandra seedlings preceded cessation of shoot elongation under short periods. Physiol Plant 95:627–632

  34. Olsen JE, Juntilla O, Nilsen J, Eriksson ME, Inger M, Olsson O, Sandberg G, Moritz T (1997) Ectopic expression of oat phytochrome A in hybrid aspen changes critical daylength for growth and prevents cold acclimatization. Plant J 12:1339–1350

  35. Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80

  36. Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Gene Dev 11:3194–3205

  37. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

  38. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS family in Arabidopsis: Sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

  39. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ Jr, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) The path forward for biofuels and biomaterials. Science 311:484–489

  40. Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Benlloch R, Nilsson O, Thomas SG, Hedden P, Phillips AL (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20:2420–2436

  41. Rinne PLH, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjarvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-Inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146

  42. Schomburg FM, Bizzell CM, Lee DJ, Zeevaart JAD, Amasino RM (2002) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15:1–13

  43. Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12:57–62

  44. Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048

  45. Webster T (2002) Dwarfing rootstocks: past, present and future. Compact Fruit Tree 35:67–72

  46. Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100

  47. Yuceer C, Kubiske ME, Harkess RL, Land SB (2003) Effects of induction treatments on flowering in Populus deltoides. Tree Physiol 23:489–495

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Acknowledgments

This work was supported in part by grants from the US Department of Energy (DOE), Poplar Genome Based Research for Carbon Sequestration in Terrestrial Ecosystems (DE-FG02-06ER64185, DE-FG02-05ER64113), the Consortium for Plant Biotechnology Research, Inc. (GO12026-203A), the United States Department of Agriculture (USDA) CSREES, the USDA-NRI Plant Genome program (2003-04345) and USDA CSREES, the Biotechnology Risk Assessment Research Grants Program (2004-35300-14687), Plant Feedstock Genomics for Bioenergy: A Joint Research Program of USDA and DOE (2009-65504-05767), industrial members of the Tree Genomics and Biosafety Research Cooperative at Oregon State University.

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Correspondence to Victor Busov.

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Zawaski, C., Kadmiel, M., Pickens, J. et al. Repression of gibberellin biosynthesis or signaling produces striking alterations in poplar growth, morphology, and flowering. Planta 234, 1285–1298 (2011). https://doi.org/10.1007/s00425-011-1485-x

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Keywords

  • Hormones
  • Populus
  • Growth
  • Gibberellin