Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-01T09:48:01.942Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluating biological containment strategies for pollen-mediated gene flow

Published online by Cambridge University Press:  08 December 2010

Alexandra Hüsken ,
Sabine Prescher  and
Joachim Schiemann

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.

Several biological containment methods have been developed to reduce pollen dispersal; many of them only have a proof of concept in a model plant species. This review focuses on biological containment measures which were tested for their long-term efficiency at the greenhouse or field scale level, i.e. plastid transformation, transgene excission, cleistogamy and cytoplasmic male sterility (CMS). Pollen-mediated gene transfer in transplastomic tobacco could occur at very low frequencies if the predominant mode of inheritance is maternal. Transgene excision from tobacco pollen can be made highly efficient by coexpression of two recombinases. For cleistogamous oilseed rape it was shown that some flowers were partially open depending on genotypes, environment and recording dates. Reports on the stability of CMS in maize and sunflower indicated that there is a high variability for different genotypes under different environmental conditions and over successive years. But for both crop types some stable lines could be selected. These data demonstrate that the biological containment methods discussed are very promising for reducing gene flow but that no single containment strategy provides 100% reduction. However, the necessary efficiency of biological containment methods depends on the level of containment required. The containment level may need to be higher for safety purposes (e.g. production of special plant-made pharmaceuticals), while much lower containment levels may already be sufficient to reach coexistence goals. It is concluded that where pollen-mediated gene flow must be prevented altogether, combinations of complementary containment systems will be required.

Keywords

biological containmentbiosafetycleistogamycytoplasmic male sterility, plastid transformationtransgene excision
Type
Review Article
Information
Environmental Biosafety Research , Volume 9 , Issue 2 , April 2010 , pp. 67 - 73
Copyright
© ISBR, EDP Sciences, 2010

References

Allainguillaume, J, Harwood, T, Ford, CS, Cuccato, G, Norris, C, Allender, CJ, Welters, R, King, GJ, Wilkinson, MJ (2009) Rapeseed cytoplasm gives advantage in wild relatives and complicates genetically modified crop biocontainment. New Phytol. 183: 1201–1211 Google ScholarPubMed
Avni, A, Edelmann, M (1991) Direct selection for paternal inheritance of chloroplasts in sexual progeny of Nicotiana. Mol. Gen. Genet. 225: 273–277 Google ScholarPubMed
Azhagiri, AK, Maliga, P (2007) Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants. Plant J. 52: 817–823 Google Scholar
Benitez, ER, Khan, NA, Matsumura, H, Abe, J, Takahas, R (2010) Varietal differences and morphology of cleistogamy in soybean. Crop Sci. 50: 185–190 Google Scholar
Birky, CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: Mechanisms and evolution. Proc. Natl. Acad. Sci. USA 92: 11331–11338 Google ScholarPubMed
Bock, R, Khan, MS (2004) Taming plastids for a green future. Trends Biotechnol. 22: 311–318 Google ScholarPubMed
Bock, R, Timmis, JN (2008) Reconstructing evolution: gene transfer from plastids to the nucleus. Bioassays 30: 556–566 Google ScholarPubMed
Budar, F, Touzet, P, De Paepe, R (2003) The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117: 3–16 Google ScholarPubMed
Chase, CD (2006) Genetically engineered cytoplasmic male sterility. Trends Plant Sci. 11: 7–9 Google ScholarPubMed
Chase, CD (2007) Cytoplasmic male sterility: a window to the world of plantmitochon-drial-nuclear interaction. Trends Genet. 23: 81–90 Google Scholar
Chase CD, Gabay-Laughnan S (2004) Cytoplasmic male sterility and fertility restoration by nuclear genes. In Daniell H, Chase CD, eds, Molecular Biology and Biotechnology of Plant Organelles, Springer, New York, pp 593–622
Cilier, M, Feruzan, D, Göksel, O (2004) Histological aspects of anther wall in male fertile and cytoplasmic male sterile Helianthus annuus L. Asi. J. Plant Sci. 3: 145–150 Google Scholar
Connor, HE (1979) Breeding systems in the grasses: a survey. New Zealand Journal of Botany 17: 547–574 Google Scholar
Conner, AJ, Glare, TR, Nap, JP (2003) The release of genetically modified crops into the environment – Part II. Overview of ecological risk assessment. Plant J. 33: 19–46 Google Scholar
Cummins, JE (1998) Chloroplast-transgenic plants are not a gene flow panacea. Nat. Biotechnol. 16: 401 Google Scholar
Daniell, H (2002) Molecular strategies for gene containment in transgenic crops. Nat. Biotechnol. 20: 581–586 Google ScholarPubMed
Daniell, H, Kumar, S, Dufourmantel, N (2005) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol. 23: 238–245 Google Scholar
De Maagd RA, Boutilier K (2009) Efficacy of strategies for biological containment of transgenic crops. A literature review. Plant Research International, Note 650
DeCosa, B, Moar, W, Lee, SB, Miller, M, Daniell, H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat. Biotechnol. 19: 71–74 Google Scholar
Den Nijs HCM, Bartsch D, Sweet J (eds) (2004) Introgression from genetically modified plants into wild relatives. CABI, p 432
Derepas, A, Dulieu, H (1992) Inheritance of the capacity to transfer plastids by the pollen parent in Petunia hybrida hort. Heredity 83: 6–10 Google Scholar
Diaz, A, MacNair, MR (1998) The effect of plant size on the expression of cleistogamy in Mimulus nasutus. Funct. Ecol. 12: 92–98 CrossRefGoogle Scholar
Dong, J, Wagner, DB (1994) Paternally inherited chloroplast polymorphism in Pinus: estimation of diversity and population subdivision, and tests of disequilibrium with maternally inherited mitochondrial polymorphism. Genetics 136: 1187–1194 Google ScholarPubMed
Dunwell JC, Ford CS (2005) Technologies for biological containment of GM- and non-GM-crops. Final Report, Defra Contract CBEC 47
EFSA (2009) Scientific opinion on guidance for the risk assessment of genetically modified plants used for non-food or non-feed purposes. EFSA Journal 1164: 1–42
Fan, ZG, Stefansson, BR (1986) Influence of temperature on sterility of 2 cytoplasmic male-sterility systems in rape (Brassica napus L.). Can J. Plant Sci. 66: 221–227 Google Scholar
Gealy DR (2005) Gene movement between rice (Oryza sativa) and weedy rice (Oryza sativa): a U.S. temperate rice perspective. In Gressel J., ed, Crop Ferality and Volunteerism, CRC Press
Gidoni, D, Srivastava, V, Carmi, N (2008) Site-specific excisional recombination strategies for elimination of undesirable transgenes from crop plants. In Vitro Cell Dev. Biol. - Plant 44: 457–467 Google Scholar
Gressel, J, Al-Ahmad, H (2005) Assessing and managing biological risks of plants used for bioremediation, including risks of transgene flow. Z. Nat. forsch. 60c: 154–165 Google Scholar
Gressel, J, Valverde, BE (2009) A strategy to provide long-term control of weedy rice while mitigating herbicide resistance transgene flow, and its potential use for other crops with related weeds. Pest. Manag. Sci. 65: 723–731 Google ScholarPubMed
Grevich, JJ, Daniell, H (2005) Chloroplast genetic engineering: Recent advances and future perspectives. Crit. Rev. Plant Sci. 24: 83–107 Google Scholar
Havey M (2004) The use of cytoplasmic male-sterility in hybrid seed production. In Daniell H, Chase C, eds, Molecular Biology and Biotechnology of Plant Organelles, Springer, New York, pp 623–634
Haygood, RA, Ives, AR, Andow, DA (2004) Population genetics of transgene containment. Ecol. Lett. 7: 213–220 Google Scholar
Hoshikawa K (1993) Anthesis, fertilization and development of caryopsis. In Matsuo T, Hoshikawa K, eds, Science of the rice plant, vol. 1 (Morphology), Food and Agriculture Policy Research Center, Nobunkyo Publ. Co, Tokyo, pp 339–376
Hüsken, A, Dietz-Pfeilstetter, A (2007) Pollen-mediated gene flow from herbicide-resistant oilseed rape (Brassica napus L.). Trans. Res. 16: 557–569 Google Scholar
Hvarleva, T, Hristova, M, Bakalova, A, Hristov, M, Atanossov, I, Atanassov, A (2009) CMS lines for evaluation of pollen flow in sunflower relevance for transgene flow mitigation. Biotechnol. Biotechnol. Equip. 23: 1309–1315 Google Scholar
Kriete, G, Niehaus, K, Perlick, AM, Puhler, A, Broer, I (1996) Male sterility in transgenic tobacco plants induced by tapetum-specific deacetylation of the externally applied non-toxic compound N-acetyl-L-phosphinothricin. Plant J. 9: 809–818 Google ScholarPubMed
Kuraichi, N, Makino, T, Hirose, S (1994) Inheritance of cleistogamy-chasmogamy in barley. Barley Genet. Newsl. 23: 19 Google Scholar
Latha, R, Thiyagarajan, K, Senthilvel, S (2004) Genetics, fertility behavior and molecular marker analysis of a new TGMS line, TS6, in rice. Plant Breed. 123: 235–240 Google Scholar
Leflon M, Pinochet X, Hüsken A, Pendergast D, Knightly S (2009a) Cleistogamy of oilseed rape: a way to prevent pollen flow at the field scale ? In 5th ISHS International Symposium on Brassicas, Programme and Abstract Book, Lillehammer, Norway
Leflon, M, Hüsken, A, Njontje, C, Knightly, S, Pendergast, D, Pierre, J, Renard, M, Pinochet, X (2009b) Stability of the cleistogamous trait during the flowering period of oilseed rape. Plant Breed. 129: 13–18 Google Scholar
Lu, BR (2003) Transgene containment by molecular means – is it possible and cost effective? Environ. Biosafety Res. 2: 3–8 Google Scholar
Lu, BR (2008) Transgene escape from GM crops and potential biosafety consequences: An anvironmental perspective. Coll. Biosafety Reviews 4: 66–141 Google Scholar
Lu YH, Belcram H, Rouault P, Piel N, Lucas MO, Falentin C, Renard M, Chalhoub B, Delourme R (2008) Cloning of a cleistogamy gene Clg1 in oilseed rape (B. napus L). In 5th ISHS International Symposium on Brassicas, Programme and Abstract Book, Lillehammer, Norway
Luo, K, Duan, H, Zhao, D, Zheng, X, Deng, W, Chen, Y, Stewart, Jr CN, McAvoy, R, Jiang, X, Wu, Y, He, A, Pei, Y, Li, Y (2007) ‘GM-gene-deletor’: Fused loxP-FRT recognition sequences dramatically improve the efficiency of FLP or CRE recombinase on transgene excision from pollen and seed of tobacco plants. Plant Biotechnol. J. 5: 263–274 Google Scholar
Marshall, DR, Thomson, NJ, Nichols, GH, Patrick, CM (1974) Effects of temperature and day length on cytoplasmic male sterility in Cotton (Gossypium). Aust. J. Agric. Res. 25: 443–450 CrossRefGoogle Scholar
Medgyesy, P, Menczel, L, Maliga, P (1980) The use of cytoplasmic streptomycin resistance: chloroplast transfer from Nicotiana tabacum into Nicotiana sylvestris, and isolation of their somatic hybrids. Mol. Gen. Genet. 179: 693–698 Google Scholar
Medgyesy, P, Páy, A, Márton, L (1986) Transmission of paternal chloroplasts in Nicotiana. Mol. Gen. Genet. 204: 195–198 Google Scholar
Miyashita, K, Matsuda, H, Ohara, M, Misawa, T, Shimamoto, Y (1999) Flowering and fruiting dynamics of chasmogamous and cleistogamous flowers in wild and cultivated soybeans. Res. Bul. Univ. Farm 31: 41–48 Google Scholar
Mlynárová, L, Conner, A, Nap, JP (2006) Directed microspore-specific recombination of transgenic alleles to prevent pollen-mediated transmission of transgenes. Plant Biotechnol. J. 4: 445–452 Google Scholar
Munsch, M, Camp, KH, Stamp, P, Weider, C (2008) Modern maize hybrids can improve grain yield as plus-hybrids by the combined effects of cytoplasmic male sterility and allo-pollination. Maydica 53: 262–268 Google Scholar
Munsch, M, Stamp, P, Christov, NK, Foueillassar, XM, Hüsken, A, Camp, KH, Weider, C (2010) Grain yield increase and pollen containment by Plus-Hybrids could improve acceptance of transgenic maize. Crop Sci. 50: 909–919 Google Scholar
Murphy, DJ (2007) Improving containment strategies in biopharming. Plant Biotechnol J. 5: 555–569 Google Scholar
Nagao, S, Takahashi, M (1963) Trial construction of twelve linkage groups in Japanese rice. Genetical studies on rice plants. J. Fac. Agr. Hokkaido Univ. 53: 72–130 Google Scholar
Pelletier, G, Budar, F (2007) The molecular biology of cytoplasmically inherited male sterility and prospects for its engineering. Curr. Opin. Biotechnol. 18: 121–125 Google ScholarPubMed
Perez-Prat, E, van Lockeren Campagne, MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci. 7: 199–203 Google ScholarPubMed
Peterson, CE, Foskett, RL (1953) Occurrence of pollen sterility in seed fields of Scott County Globe onions. Proc. Am. Soc. Hort. Sci. 62: 443–448 Google Scholar
Peterson, G, Cunningham, S, Deutsch, L, Erikson, J, Quinlan, A, Raez-Luna, E, Tinch, R, Troell, M, Woodburg, P, Zens, S (2000) The risks and benefits of genetically modified crops: a multidisciplinary perspective. Conserv. Ecol. 4: 13 Google Scholar
Quesada-Vargas, T, Ruiz, ON, Daniell, H (2005) Characterization of heterologous multigene operons in transgenic chloroplasts. Plant Physiol. 138: 1746–1762 Google Scholar
Ruf, S, Karcher, D, Bock, R (2007) Determining the transgene containment level provided by chloroplast transformation. Proc. Natl. Acad. Sci. USA 104: 6998–7002 Google ScholarPubMed
Ruiz, O, Daniell, H (2005) Cytoplasmic male sterility engineered via the plastid genome. Plant Physiol. 138: 1232–1246 Google Scholar
Sarvella, P (1966) Environmental influences on sterility in cytoplasmic male-sterile cottons. Crop Sci. 6: 361–364 Google Scholar
Sawhney, VK (2004) Photoperiod-sensitive male sterile mutant in tomato and its potential use in hybrid seed production. J. Hortic. Sci. Biotech. 79: 138–141 Google Scholar
Sheppard, AE, Ayliffe, MA, Blatch, L, Day, A, Delaney, SK, Khairul-Fahmy, N, Li, Y, Madesis, P, Pryor, AJ, Timmis, JN (2008) Transfer of plastid DNA to the nucleus is elevated during male gametogenesis in tobacco. Plant Phys. 148: 328–336 Google ScholarPubMed
Stamp, P, Chowchong, S, Menzi, M, Weingartner, U, Kaeser, O (2000) Increase in the yield of cytoplasmic male sterile maize revisited. Crop Sci. 40: 1586–1587 Google Scholar
Stegemann, S, Bock, R (2006) Experimental reconstruction of functional gene transfer from the tobacco plastid genome to the nucleus. Plant Cell 18: 2869–2878 Google ScholarPubMed
Svab, Z, Maliga, P (2007) Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc. Natl. Acad. Sci. USA 104: 7003–7008 Google Scholar
Testolin, R, Cipriani, G (1997) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in the genus Actinidia. Theor. Appl. Genet. 94: 897–903 Google Scholar
Turuspekov, Y, Honda, I, Watanabe, Y, Stein, N, Komatsuda, T (2009) An inverted and micro-colinear genomic regions of rice and barley carrying the cly1 gene for cleistogamy. Breed. Science 59: 657–663 Google Scholar
Wang, T, Li, Y, Shi, Y, Reboud, X, Darmency, H, Gressel, J (2004) Low frequency transmission of a plastid-encoded trait in Setaria italica. Theor. Appl. Genet. 108: 315–320 Google Scholar
Weingartner, U, Kaeser, O, Long, M, Stamp, P (2002) Combining cytoplasmic male sterility and xenia increases grain yield of maize hybrids. Crop Sci. 42: 1848–1856 Google Scholar
Weider, C, Stamp, P, Christov, N, Hüsken, A, Foueillassar, X, Camp, KH, Munsch, M (2009) Stability of cytoplasmic male sterility in maize under different environmental conditions. Crop Sci. 49: 77–84 Google Scholar
Yoshida, G, Itoh, JI, Ohmori, S, Miyoshi, K, Horigome, A, Uchida, E, Kimizu, M, Matsumura, Y, Kusaba, M, Satoh, H, Nagato, Y (2007) Superwoman1-cleistogamy, a hopeful allele for gene containment in GM-rice. Plant Biotechnol. J. 5: 1–12 Google Scholar