Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-01T20:08:14.426Z Has data issue: false hasContentIssue false
  • English
  • Français

Developing risk hypotheses and selecting species for assessingnon-target impacts of GM trees with novel traits: The case of altered-lignin pinetrees

Published online by Cambridge University Press:  15 November 2011

Louise A. Malone ,
Jacqui H. Todd ,
Elisabeth P. J. Burgess ,
Christian Walter ,
Armin Wagner  and
Barbara I.P. Barratt
Louise A. Malone*
Affiliation:
The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research), Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand
Jacqui H. Todd
Affiliation:
The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research), Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand
Elisabeth P. J. Burgess
Affiliation:
The New Zealand Institute for Plant & Food Research Limited (Plant & Food Research), Mt Albert, Private Bag 92169, Auckland Mail Centre, Auckland 1142, New Zealand
Christian Walter
Affiliation:
The New Zealand Forest Research Institute Limited (Scion), Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua Mail Centre, Rotorua 3046, New Zealand
Armin Wagner
Affiliation:
The New Zealand Forest Research Institute Limited (Scion), Te Papa Tipu Innovation Park, Private Bag 3020, Rotorua Mail Centre, Rotorua 3046, New Zealand
Barbara I.P. Barratt
Affiliation:
AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand
*
∗ Corresponding author:louise.malone@plantandfood.co.nz

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

A procedure is presented for developing environmental risk hypotheses associated with thedeployment of forest trees genetically modified to have altered wood properties and forselecting non-target species to test these hypotheses. Altered-lignin Pinusradiata trees intended for use in New Zealand are used as a hypothetical casestudy to illustrate our approach. Firstly, environmental management goals (such as woodproduction, flood control or preservation of biodiversity) were identified and linked tothe forest attributes they require. Necessary conditions for each attribute were listedand appropriate assessment endpoints for them developed. For example, biological controlof pests may be one condition necessary for a forest to have healthy trees, and thediversity and abundance of natural enemy species in the forest could be an appropriateassessment endpoint for measuring this condition. A conceptual model describing therelationships between an altered-lignin GM pine tree and potentially affectedinvertebrates and micro-organisms in a plantation forest was used to develop a set of riskhypotheses describing how the GM trees might affect each assessment endpoint. Becausepurified lignin does not represent the properties it imparts to wood, maximum hazard dosetests with non-target organisms, as are used to inform toxin risk assessment, cannot beconducted. Alternative experiments, based on current knowledge of the responses oforganisms to lignin, must be designed. A screening method was adapted and applied to adatabase of invertebrate species known to inhabit New Zealand pine forests to identify andprioritize non-target invertebrate species that could be used as experimental subjects forexamining these hypotheses. The screening model and its application are presented, alongwith a set of recommendations for pre-release tests with GM pines and potentially affectedinvertebrates and micro-organisms.

Keywords

genetically modified treesaltered ligninnon-target invertebratesecological risk assessment
Type
Research Article
Information
Environmental Biosafety Research , Volume 9 , Issue 4 , October 2010 , pp. 181 - 198
Copyright
© ISBR, EDP Sciences, 2011

References

Andow, DA (2011) Assessing unintended effects of GM plants on biological species. J. Verbr. Lebensm. 6 (Suppl 1): S119–S124 Google Scholar
Andow, DA, Hilbeck, A (2004) Science-based risk assessment for nontarget effects of transgenic crops. Bioscience 54: 637–649 Google Scholar
Andow DA, Hilbeck A, Nguyen Van Tuat (2008) Environmental Risk Assessment of Genetically Modified Organisms. Volume 4. Challenges and opportunities with Bt cotton in Vietnam. Oxford. CABI International
Anon (2005a) B/BE/07/V2Belgian Biosafety Server
Anon (2005b) Land use by farm type. Ministry of Agriculture and Forestry. http://www.maf.govt.nz/statistics/land-use/
Anon (2007) Notification report, B/BE/07/VE, 30/11/2007. European Commission Joint Research Centre, Institute for Health and Consumer Protection. http://gmoinfo.jrc.ec.europa.eu/gmp_ report.aspx?CurNot=B/BE/07/V2
Anon (2008) Advice of the Belgian Biosafety Advisory Council on the notification of B/BE/07/V2 of the VIB, Flanders Institute of Biotechnology, for deliberate release in the environment of genetically modified poplars with an altered wood composition for research and development. WIV-ISP/BAC/2008_733. 25/04/2008. http://www.bio-council.be/bac_advices.html; http://www.bio-council.be/docs/BAC_2008_ 733.pdf
Axelsson, EP, Hjaltan, J, Leroy, CJ, Julkunen-Tiitto, R, Wennstrom, A, Pilate, G (2010) Can leaf litter from genetically modified trees affect aquatic ecosystems? Ecosystems 13: 1049–1059 Google Scholar
Barraclough, EI, Burgess, EPJ, Philip, BA, Wohlers, MW, Malone, LA (2009) Tri-trophic impacts of Bt-expressing transgenic pine on the parasitoid Meteorus pulchricornis (Hymenoptera: Braconidae) via its host Pseudocoremia suavis (Lepidoptera: Geometridae). Biol. Control 49: 192–199 Google Scholar
Barratt BIP, Todd JH, Burgess EPJ, Malone LA Developing biosafety risk hypotheses for invertebrates exposed to GM plants using conceptual food webs: a case study with elevated triacylglyceride levels in ryegrass. Environ. Biosafety Res., in press
Benge J, Moller H, Logan D (2006) Cicada species in kiwifruit orchards. ARGOS Research Note [online] www.argos.org.nz
Bishop-Hurley, SL, Zabkiewicz, RJ, Grace, L, Gardner, RC, Wagner, A, Walter, C (2001) Conifer genetic engineering: transgenic Pinus radiata (D. Don) and Picea abies (Karst) plants are resistant to the herbicide Buster. Plant Cell Rep. 20: 235–243 Google Scholar
Boerjan, W, Ralph, J, Baucher, M (2003) Lignin biosynthesis. Annu. Rev. Plant Biol. 54: 519–546 Google ScholarPubMed
Bradley, KL, Hancock, JE, Giardina, CP, Pregitzer, KS (2007) Soil microbial community responses to altered lignin biosynthesis in Populus tremuloides vary among three distinct soils. Plant Soil 294: 185–201 Google Scholar
Chuchou, M, Grace, LJ (1983) Characterization and identification of mycorrhizas of radiata pine in New Zealand. Australian Forest Research 13: 121–132 Google Scholar
Chuchou, M, Grace, LJ (1988) Mycorrhizal fungi of radiata pine in different forests of the North and South Islands in New Zealand. Soil Biol. Biochem. 20: 883–886 Google Scholar
Chuchou, M, Grace, LJ (1990) Mycorrhizal fungi of radiata pine seedlings in nurseries and trees in forests. Soil Biol. Biochem. 22: 959–966 Google Scholar
Clissold, FJ, Sanson, GD, Read, J, Simpson, SJ (2009) Gross vs. net income: How plant toughness affects performance of an insect herbivore. Ecology 90: 3393–3405 Google Scholar
Colbourne, R, Kleinpaste, R (1983) A banding study of North Island brown kiwis in an exotic forest. Notornis 30: 109–124 Google Scholar
Cowley, DR (1978) Studies on the larvae of New Zealand Trichoptera. N. Z. J. Zool. 5: 639–750 Google Scholar
Crane, PE, Hopkins, AJM, Dick, MA, Bulman, LS (2009) Behaviour of Neonectria fuckeliana causing a pine canker disease in New Zealand. Can. J. For. Res.-Rev. Can. Rech. For. 39: 2119–2128 Google Scholar
Dennis J, Kaplan I, Chu A (2005) Production and markets. In Colley M, ed, New Zealand Institute of Forestry Inc. Forestry Handbook. Tauranga, New Zealand, Design & Print Management Ltd, pp 190–192
ERMANZ, Environmental Risk Management Authority New Zealand (2010) Application for field testing genetically modified organisms in containment under section 40(1)(c) of the HSNO Act 1996. In: New Zealand Forest Research Institute Ltd taS (Ed.) Field Test in Containment Genetically Modified Pine Trees. Wellington, New Zealand, ERMANZ. pp. 57
EFSA, European Food Safety Authority (2010a) EFSA Panel on Genetically Modified Organisms (GMO); Guidance on the environmental risk assessment of genetically modified plants. EFSA J. 8(11):1879. [111 pp.]. doi:10.2903/j.efsa.2010.1879
EFSA, European Food Safety Authority (2010b) EFSA Panel on Genetically Modified Organisms (GMO); Scientific opinion on the environmental risk assessment of genetically modified plants. EFSA J. 8(11):1877 [72 pp.]. doi:10.2903/j.efsa.2010.1877
Ferraz, A, Rodriguez, J, Freer, J, Baeza, J (2001) Biodegradation of Pinus radiata softwood by white- and brown-rot fungi. World J. Microbiol. Biotechnol. 17: 31–34 Google Scholar
Ferreira, SA, Pitz, KY, Manshardt, R, Zee, F, Fitch, M, Gonsalves, D (2002) Virus coat protein transgenic papaya provides practical control of Papaya ringspot virus in Hawaii. Plant Dis. 86: 101–105 Google Scholar
Ferrer, M, Beloqui, A, Golyshin, PN (2010) Screening metagenomic libraries for laccase activities. Methods Mol. Biol. 668: 189–202 Google ScholarPubMed
Find, JI, Charity, JA, Grace, LJ, Kristensen, MMMH, Krogstrup, P, Walter, C (2005) Stable genetic transformation of embryogenic cultures of Abies nordmanniana (Nordmann fir) and regeneration of transgenic plants. In Vitro Cell. Dev. Biol.Plant 41: 725–730 Google Scholar
Franich, RA, Carson, MJ, Carson, SD (1986) Synthesis and accumulation of benzoic acid in Pinus radiata needles in response to tissue injury by dothistromin, and correlation with resistance of Pinus radiata families to Dothistroma pini. Physiol. Mol. Plant Pathol. 28: 267–286 Google Scholar
Garrett, LG, Kimberley, MO, Oliver, GR, Pearce, SH, Paul, TSH (2010) Decomposition of woody debris in managed Pinus radiata plantations in New Zealand. For. Ecol. Manag. 260: 1389–1398 Google Scholar
Geib, SM, Filley, TR, Hatcher, PG, Hoover, K, Carlson, JE, Jimenez-Gasco, MD, Nakagawa-Izumi, A, Sleighter, RL, Tien, M (2008) Lignin degradation in wood-feeding insects. Proc. Natl. Acad. Sci. U. S. A. 105: 12932–12937 Google ScholarPubMed
Grabber, JH, Schatz, PF, Kim, H, Lu, F, Ralph, J (2010) Identifying new lignin bioengineering targets: 1. Monolignol-substitute impacts on lignin formation and cell wall fermentability. BMC Plant Biology 10: 114 Google ScholarPubMed
Grace, LJ, Charity, JA, Gresham, B, Kay, N, Walter, C (2005) Insect-resistant transgenic Pinus radiata. Plant Cell Rep. 24: 103–111 Google ScholarPubMed
Hancock, JE, Bradley, KL, Giardina, CP, Pregitzer, KS (2008) The influence of soil type and altered lignin biosynthesis on the growth and above and belowground biomass allocation of Populus tremuloides. Plant Soil 308: 239–253 Google Scholar
Henault, C, English, LC, Halpin, C, Andreux, F, Hopkins, DW (2006) Microbial community structure in soils with decomposing residues from plants with genetic modifications to lignin biosynthesis. FEMS Microbiol. Lett. 263: 68–75 Google ScholarPubMed
Hilbeck A, Andow DA (2004) Environmental Risk Assessment of Genetically Modified Organisms. Volume 1. A case study of Bt maize in Kenya. Oxford. CABI International
Hilbeck A, Andow DA, Fontes EMG (2006) Environmental Risk Assessment of Genetically Modified Organisms. Volume 2. Methodologies for assessing Bt cotton in Brazil. Oxford. CABI International
Hitchmough R (comp.) (2002) New Zealand Threat Classification System lists – 2002. Threatened species occasional publication 23, Department of Conservation, Wellington, New Zealand
Hood, IA, Kimberley, MO, Gardner, JF (2009) Susceptibility to Armillaria novae-zelandiae among clones of Pinus radiata. For. Pathol. 39: 405–414 Google Scholar
Hotter, GS (1997) Elicitor-induced oxidative burst and phenylpropanoid metabolism in Pinus radiata cell suspension cultures. Aust. J. Plant Physiol. 24: 797–804 Google Scholar
Huang, DF, Zhang, J, Song, FP, Lang, ZH (2007) Microbial control and biotechnology research on Bacillus thuringiensis in China. J. Invertebr. Pathol. 95: 175–180 Google Scholar
Huntley, SK, Ellis, D, Gilbert, M, Chapple, C, Mansfield, SD (2003) Significant increases in pulping efficiency in C4H-F5H-transformed poplars: Improved chemical savings and reduced environmental toxins. J. Agric. Food Chem. 51: 6178–6183 Google ScholarPubMed
Johnson, SN, Hallett, PD, Gillespie, TL, Halpin, C (2010) Below-ground herbivory and root toughness: a potential model system using lignin-modified tobacco. Physiol. Entomol. 35: 186–191 Google Scholar
Kim, KW, Lee, IJ, Thoungchaleun, V, Kim, CS, Lee, DK, Park, EW (2009) Visualization of wound periderm and hyphal profiles in pine stems inoculated with the pitch canker fungus Fusarium circinatum. Microsc. Res. Tech. 72: 965–973 Google ScholarPubMed
Lahtinen, M, Kruus, K, Heinonen, P, Sipila, J (2009) On the reactions of two fungal laccases differing in their redox potential with lignin model compounds: products and their rate of formation. J Agric Food Chem 57: 8357–8365 Google ScholarPubMed
Levee, V, Major, I, Levasseur, C, Tremblay, L, MacKay, J, Seguin, A (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol. 184: 48–70 Google Scholar
Lottmann, J, O’Callaghan, M, Baird, D, Walter, C (2010) Bacterial and fungal communities in the rhizosphere of field-grown genetically modified pine trees (Pinus radiata D.). Environ. Biosafety Res. 9: 25–40 Google Scholar
Miller D (1971) Common Insects in New Zealand. Wellington, A.H. & A.W. Reed Ltd
Milligan RH (1978) Hylastes ater (Paykull) (Coleoptera: Scolytidae). Black pine bark beetle. New Zealand Forest Service, Forest and Timber Insects in New Zealand 29
Morgan, FD (1959) The ecology and external morphology of Stolotermes ruficeps Brauer (Isoptera: Hodotermitidae). Trans. Roy. Soc. N. Z. 86: 155–195 Google Scholar
Nanayakkara, B, Manley-Harris, M, Suckling, ID, Donaldson, LA (2009) Quantitative chemical indicators to assess the gradation of compression wood. Holzforschung 63: 431–439 Google Scholar
Parfitt, RL, Newman, RH (2000) 13C NMR study of pine needle decomposition. Plant Soil 219: 273–278 Google Scholar
Parkinson B (2007) A photographic guide to the insects of New Zealand. Auckland, New Holland Publishers (NZ) Ltd
Pawson, SM, Ecroyd, CE, Seaton, R, Shaw, WB, Brockerhoff, EG (2010) New Zealand’s exotic plantation forests as habitats for threatened indigenous species. N. Z. J. Ecol. 34: 342–355 Google Scholar
Peeters, PJ, Sanson, G, Read, J (2007) Leaf biomechanical properties and the densities of herbivorous insect guilds. Funct. Ecol. 21: 246–255 Google Scholar
Pilate, G, Guiney, E, Holt, K, Petit-Conil, M, Lapierre, C, Leple, JC, Pollet, B, Mila, I, Webster, EA, Marstorp, HG, Hopkins, DW, Jouanin, L, Boerjan, W, Schuch, W, Cornu, D, Halpin, C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat. Biotechnol. 20: 607–612 Google ScholarPubMed
Prins, RA, Kreulen, DA (1991) Comparative aspects of plant-cell wall digestion in insects. Anim. Feed Sci. Tech. 32: 101–118 Google Scholar
Punelli, F, Reverberi, M, Porretta, D, Nogarotto, S, Fabbri, AA, Fanelli, C, Urbanelli, S (2009) Molecular characterization and enzymatic activity of laccases in two Pleurotus spp. with different pathogenic behaviour. Mycol. Res. 113: 381–387 Google ScholarPubMed
Raybould, A, Caron-Lormier, G, Bohan, D (2011) Derivation and interpretation of hazrd quotients to assess ecological risks from the cultivation of insect-resistant transgenic crops. J. Agric. Food Chem. 59: 5877–5885 Google ScholarPubMed
Rogers, DJ, Lewthwaite, SE, Dentener, PR (2002) Rearing huhu beetle larvae, Prionoplus reticularis (Coleoptera: Cerambycidae) on artificial diet. N. Z. J. Zool. 29: 303–310 Google Scholar
Romeis, J, Hellmich, RL, Candolfi, MP, Carstens, K, De, Schrijver A,Gatehouse, AMR, Herman, RA, Huesing, JE, McLean, MA, Raybould, A, Shelton, AM, Waggoner, A (2011) Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants. Transgenic Res. 20: 1–22 Google ScholarPubMed
Schirp, A, Farrell, RL, Kreber, B (2003) Effects of New Zealand sapstaining fungi on structural integrity of unseasoned radiata pine. Holz Als Roh-und Werkst. 61: 369–376 Google Scholar
Schnitzler, F-R, Burgess, EPJ, Kean, AM, Philip, BA, Barraclough, EI, Malone, LA, Walter, C (2010) No unintended impacts of transgenic pine (Pinus radiata) trees on above-ground invertebrate communities. Environ. Entomol. 39: 1359–1368 Google ScholarPubMed
Schwelm, A, Barron, NJ, Baker, J, Dick, M, Long, PG, Zhang, S, Bradshaw, RE (2009) Dothistromin toxin is not required for dothistroma needle blight in Pinus radiata. Plant Pathol. 58: 293–304 Google Scholar
Seppanen, SK, Pasonen, HL, Vauramo, S, Vahala, J, Toikka, M, Kilpelainen, I, Setala, H, Teeri, TH, Timonen, S, Pappinen, A (2007) Decomposition of the leaf litter and mycorrhiza forming ability of silver birch with a genetically modified lignin biosynthesis pathway. Appl. Soil Ecol. 36: 100–106 Google Scholar
Stoytchev, I, Nerud, F (2000) Ligninolytic enzyme complex of Armillaria spp. Folia Microbiol. 45: 248–250 Google ScholarPubMed
Sutela, S, Niemi, K, Edesi, J, Laakso, T, Saranpaa, P, Vuosku, J, Makela, R, Tiimonen, H, Chiang, VL, Koskimaki, J, Suorsa, M, Julkunen-Tiitto, R, Haggman, H (2009) Phenolic compounds in ectomycorrhizal interaction of lignin modified silver birch. BMC Plant Biol. 9: 124 Google ScholarPubMed
Tiimonen, H, Aronen, T, Laakso, T, Saranpaa, P, Chiang, V, Haggman, H, Niemi, K (2008) Paxillus involutus forms an ectomycorrhizal symbiosis and enhances survival of PtCOMT-modified Betula pendula in vitro. Silvae Genet. 57: 235–242 Google Scholar
Tiimonen, H, Aronen, T, Laakso, T, Saranpaa, P, Chiang, V, Ylioja, T, Roininen, H, Haggman, H (2005) Does lignin modification affect feeding preference or growth performance of insect herbivores in transgenic silver birch (Betula pendula Roth)? Planta 222: 699–708 Google Scholar
Todd, JH, Ramankutty, P, Barraclough, EI, Malone, LA (2008) A screening method for prioritizing non-target invertebrates for improved biosafety testing of transgenic crops. Environ. Biosafety Res. 7: 35–56 Google ScholarPubMed
Tronchet, M, Balague, C, Kroj, T, Jouanin, L, Roby, D (2010) Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Mol. Plant Pathol. 11: 83–92 Google Scholar
Uprichard JM (1991) Chemistry of Wood and Bark. In Kininmonth JA, Whitehouse LJ, eds, Properties and Use of Radiata Pine, Vol 1 - Wood Properties. Rotorua, New Zealand, New Zealand Ministry of Forestry, Forest Research Institute
USDA (2010) Permit applications 08–011–106rm and 08–014–101rm received from ArborGen LLC. Field testing of genetically engineered Eucalyptus grandis X Eucalyptus urophylla. Final Environmental Assessment. April 2010
USEPA, United States Environmental Protection Agency (1998) Guidelines for Ecological Risk Assessment. EPA/630/R095/002F. http://cfpub.epa.gov/ncea/raf/recordisplay.cfm?deid=12460
Valenzuela, S, Balocchi, C, Rodriguez, J (2006) Transgenic trees and forestry biosafety. Electron. J. Biotechnol. 9: 335–339 Google Scholar
Vanholme, R, Morreel, K, Ralph, J, Boerjan, W (2008) Lignin engineering. Curr. Opin. Plant Biol. 11: 278–285 Google ScholarPubMed
Wagner, A, Donaldson, L, Kim, H, Phillips, L, Flint, H, Steward, D, Torr, K, Koch, G, Schmitt, U, Ralph, J (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol. 149: 370–383 Google ScholarPubMed
Wagner, A, Ralph, J, Akiyama, T, Flint, H, Phillips, L, Torr, K, Nanayakkara, B, Kiri, LT (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA : shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc. Natl. Acad. Sci. U. S. A. 104: 11856–11861 Google ScholarPubMed
Walbert, K, Ramsfield, TD, Ridgway, HJ, Jones, EE (2010) Ectomycorrhizal species associated with Pinus radiata in New Zealand including novel associations determined by molecular analysis. Mycorrhiza 20: 209–215 Google ScholarPubMed
Walter, C, Fladung, M, Boerjan, W (2010) The 20-year environmental safety record of GE trees. Nat. Biotechnol. 28: 656–658 Google Scholar
Wang, Q, Shi, GL, Song, D, Rogers, DJ, Davis, LK, Chen, XN (2002) Development, survival, body weight, longevity, and reproductive potential of Oemona hirta (Coleoptera : Cerambycidae) under different rearing conditions. J. Econ. Entomol. 95: 563–569 Google ScholarPubMed
Watt, JC (1982) New Zealand beetles. N. Z. Entomol. 7: 213–221 Google Scholar
Wilkinson, M, Tepfer, M (2009) Fitness and beyond: Preparing for the arrival of GM crops with ecologically important novel characters. Environ. Biosafety Res. 8: 1–14 Google ScholarPubMed
Williams HW (1971) Dictionary of the Maori Language, Seventh Edition. Wellington, Legislation Direct
Zhang, Z, Van, Epenhuijsen CW,Brash, D, Hosking, GP (2004) Phosphine as a fumigant to control Hylastes ater and Arhopalus ferus, pests of export logs. N. Z. Plant Protection 57: 257–259 Google Scholar