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http://dx.doi.org/10.5141/ecoenv.2013.005

Fitness cost and competitive ability of transgenic herbicide-tolerant rice expressing a protoporphyrinogen oxidase gene  

Chun, Young Jin (Department of Biology, Jeju National University)
Kim, Dae In (Bio-Evaluation Center, Korea Research Institute of Bioscience & Biotechnology)
Park, Kee Woong (Department of Crop Science, Chungnam National Unversity)
Jeong, Soon-Chun (Bio-Evaluation Center, Korea Research Institute of Bioscience & Biotechnology)
Park, Sangkyu (Division of Natural Sciences, Ajou University)
Back, Kyoungwhan (Division of Applied Bioscience and Biotechnology, Chonnam National University)
Kim, Chang-Gi (Bio-Evaluation Center, Korea Research Institute of Bioscience & Biotechnology)
Publication Information
Journal of Ecology and Environment / v.36, no.1, 2013 , pp. 39-47 More about this Journal
Abstract
The expression of transgenic traits in genetically modified crops is sometimes associated with decreases in crop performance or fitness. These decreases in performance or fitness of transgenic plants in unfavourable conditions may provide valuable information about the ecological consequences of transgene escape. In a glasshouse trial, we tested the cost associated with resistance to herbicides by comparing the growth, yield, and competitive ability of transgenic rice with its parental non-transgenic line. This new line was developed for constitutive overexpression of protoporphyrinogen oxidase (PPO) to increase resistance to herbicides. We evaluated nine agronomic traits of transgenic and non-transgenic rice grown in a replacement series design over four densities. Competitive ability was also assessed between transgenic and non-transgenic plants by analyzing their relative yields based on biomass and seed weight data. Our results indicated that non-transgenic plants showed greater performance than did the transgenic plants when those genotypes were grown in mixtures. The non-transgenic rice plants exhibited superior competitive ability at certain combinations of planting densities and genotype proportions. These results suggest that PPO-herbicide resistance incurs some costs in plant performance and competitive ability.
Keywords
biosafety; competition; resistance; protoporphyrinogen oxidase; transgenic rice;
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1 Burke JM, Rieseberg LH. 2003. Fitness effects of transgenic disease resistance in sunflowers. Science 300: 1250.   DOI   ScienceOn
2 Chapman MA, Burke JM. 2006. Letting the gene out of bottle: the population genetics of genetically modified crops. New Phytol 170: 429-443.   DOI   ScienceOn
3 Chen L-Y, Snow AA, Wang F, Lu B-R. 2006. Effects of insect-resistance transgenes on fecundity in rice (Oryza sativa, Poaceae): a test for underlying costs. Am J Bot 93: 94-101.   DOI   ScienceOn
4 Cipollini D. 2010. Constitutive expression of methyl jasmonate-inducible responses delays reproduction and constrains fitness responses to nutrients in Arabidopsis thaliana. Evol Ecol 24: 59-68.   DOI
5 Dale PJ, McPartlan HC. 1992. Field performance of transgenic potato plants compared with controls regenerated from tuber discs and shoot cuttings. Theor Appl Genet 84: 585-591.
6 Damgaard C, Kjaer C. 2009. Competitive interactions and the effect of herbivory on Bt-Brassica napus, Brassica rapa and Lolium perenne. J Appl Ecol 46: 1073-1079.   DOI   ScienceOn
7 Di K, Neal Stewart C Jr, Wei W, Shen B-C, Tang Z-X, Ma K-P. 2009. Fitness and maternal effects in hybrids formed between transgenic oilseed rape (Brassica napus L.) and wild brown mustard [B. juncea (L.) Czern et Coss.] in the field. Pest Manag Sci 65: 753-760.   DOI   ScienceOn
8 Ellstrand NC. 2003. Current knowledge of gene flow in plants: implications for transgene flow. Philos T Roy Soc B 358: 1163-1170.   DOI   ScienceOn
9 Ellstrand NC, Prentice HC, Hancock JF. 1999. Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Evol Syst 30: 539-563.   DOI   ScienceOn
10 Fowler N. 1982. Competition and coexistence in a North Carolina grassland. III. Mixtures of component species. J Ecol 70: 77-92.   DOI   ScienceOn
11 Fredshavn JR, Poulsen GS. 1996. Growth behavior and competitive ability of transgenic crops. Field Crop Res 45: 11-18.   DOI   ScienceOn
12 Fredshavn JR, Poulsen GS, Huybrechts I, Rudelsheim P. 1995. Competitiveness of transgenic oilseed rape. Transgenic Res 4: 142-148.   DOI
13 Gassmann AJ, Futuyma DJ. 2005. Consequence of herbivory for the fitness cost of herbicide resistance: photosynthetic variation in the context of plant–herbivore interactions. J Evol Biol 18: 447-454.
14 Gurr SJ, Rushton PJ. 2005. Engineering plants with increased disease resistance: how are we going to express it? Trends Biotechnol 23: 283-290.   DOI   ScienceOn
15 Hails RS. 2000. Genetically modified plants - the debate continues. Trends Ecol Evol 15: 14-18.   DOI   ScienceOn
16 Hails RS, Morley K. 2005. Genes invading new populations: a risk assessment perspective. Trends Ecol Evol 20: 245-252.   DOI   ScienceOn
17 Hails RS, Rees M, Kohn DD, Crawley MJ. 1997. Burial and seed survival in Brassica napus subsp. oleifera and Sinapis arvensis including a comparison of transgenic and non-transgenic lines of the crop. P Roy Soc Lond B-Bio 264: 1-7.   DOI   ScienceOn
18 Halfhill MD, Sutherland JP, Moon HS, Poppy GM, Warwick SI, Weissinger AK, Rufty TW, Raymer PL, Neal Stewart C Jr. 2005. Growth, productivity, and competitiveness of introgressed weedy Brassica rapa hybrids selected for the presence of Bt cry1Ac and gfp transgenes. Mol Ecol 14: 3177-3189.   DOI   ScienceOn
19 Hilder VA, Gatehouse AMR. 1991. Phenotypic cost to plants of an extra gene. Transgenic Res 1: 54-60.   DOI
20 Hsieh T-H, Lee J-T, Charng Y-Y, Chan M-T. 2002a. Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130: 618-626.   DOI   ScienceOn
21 Hsieh T-H, Lee J-T, Yang P-T, Chiu L-H, Charng Y-Y, Wang Y-C, Chan M-T. 2002b. Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129: 1086-1094.   DOI   ScienceOn
22 Inouye BD. 2001. Response surface experimental designs for investigating interspecific competition. Ecology 82: 2696-2706.   DOI   ScienceOn
23 Jackson MW, Stinchcombe JR, Korves TM, Schmitt J. 2004. Costs and benefits of cold tolerance in transgenic Arabidopsis thaliana. Mol Ecol 13: 3609-3615.   DOI   ScienceOn
24 James C. 2010. Global status of commercialized biotech/GM crops, ISAAA Briefs No. 42. ISAAA, Ithaca, New York, USA.
25 Jung HI, Kuk YI, Kim HY, Back K, Lee DJ, Lee S, Burgos NR. 2010. Resistance levels and fitness of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice in paddy fields. Field Crop Res 115: 125-131.   DOI   ScienceOn
26 Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1999. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnol 17: 287-291.   DOI   ScienceOn
27 Kim S, Kim C, Li W, Kim T, Li Y, Zaidi MA, Altossar I. 2008. Inheritance and field performance of transgenic Korean Bt rice lines resistant to rice yellow stem borer. Euphytica 164: 829-839.   DOI
28 Lavigne C, Manac’h H, Guyard C, Gasquez J. 1995. The cost of herbicide resistance in white-chicory: ecological implications for its commercial release. Theor Appl Genet 91: 1301-1308.
29 McHughen A, Holm F. 1991. Herbicide resistant transgenic flax field test: agronomic performance in normal and sulfonylurea-containing soils. Euphytica 55: 49-56.   DOI
30 Ortelli S, Winzeler H, Winzeler M, Fried PM, Nosberger J. 1996. Leaf rust resistance gene Lr9 and winter wheat yield reduction: I. Yield and yield components. Crop Sci 36: 1590-1595.   DOI
31 Owen MD, Zelaya IA. 2005. Herbicide-resistant crops and weed resistance to herbicides. Pest Manag Sci 61: 301-311.   DOI   ScienceOn
32 Pasonen H-L, Vihervuori L, Seppanen S-K, Lyytikainen-Saarenmaa P, Ylioja T, von Weissenberg K, Pappinen A. 2008. Field performance of chitinase transgenic silver birch (Betula pendula Roth): growth and adaptive traits. Trees Struct Funct 22: 413-421.   DOI   ScienceOn
33 Plowman AB, Richards AJ. 1997. The effect of light and temperature on competition between atrazine susceptible and resistant Brassica rapa. Ann Bot 80: 583-590.   DOI   ScienceOn
34 Purrington CB, Bergelson J. 1997. Fitness consequences of genetically engineered herbicide and antibiotic resistance in Arabidopsis thaliana. Genetics 145: 807-814.
35 Ramachandran S, Buntin GD, All JN, Raymer PL, Neal Stewart C Jr. 2000. Intraspecific competition of an insect-resistant transgenic canola in seed mixtures. Agron J 92: 368-374.   DOI
36 Regal PJ. 1988. The adaptive potential of genetically engineered organisms in nature. Trends Ecol Evol 3: S36S38.
37 Romeis J, Waldburger M, Streckeisen P, Hogervorst PAM, Keller B, Winzeler M, Bigler F. 2007. Performance of transgenic spring wheat plants and effects on non-target organisms under glasshouse and semi-field conditions. J Appl Entomol 131: 593-602.   DOI   ScienceOn
38 Sasu MA, Ferrari MJ, Du D, Winsor JA, Stephenson AG. 2009. Indirect costs of a nontarget pathogen mitigate the direct benefits of a virus-resistant transgene in wild Cucurbita. P Natl Acad Sci USA 106: 19067-19071.   DOI   ScienceOn
39 Snow AA, Pilson D, Rieseberg LH, Paulsen MJ, Pleskac N, Reagon MR, Wolf DE, Selbo SM. 2003. A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol Appl 13: 279-286.   DOI   ScienceOn
40 Snow AA, Andersen B, Jorgensen RB. 1999. Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa. Mol Ecol 8: 605-615.   DOI   ScienceOn
41 Vacher C, Weis AE, Hermann D, Kossler T, Young C, Hochberg ME. 2004. Impact of ecological factors on the initial invasion of Bt transgenes into wild populations of birdseed rape (Brassica rapa). Theor Appl Genet 109: 806-814.   DOI
42 Warwick SI. 2007. Gene flow between GM crops and related species in Canada. In: The First Decade of Herbicide Resistant Crops in Canada (Swanton C, Gulden R, eds), Topics in Canadian Weed Science, vol 4. Canadian Weed Science Society, pp 101-113.
43 Warwick SI, Black LD. 1994. Relative fitness of herbicide-resistant and -susceptible biotypes of weeds. Phytoprotection 75: 37-49.   DOI
44 Warwick SI, Legere A, Simard M-J, James T. 2008. Do escaped transgenes persist in nature? The case of an herbicide resistance transgene in a weedy Brassica rapa population. Mol Ecol 17: 1387-1395.   DOI   ScienceOn
45 Warwick SI, Beckie HJ, Hall LM. 2009. Gene flow, invasiveness, and ecological impact of genetically modified crops. Ann NY Acad Sci 1168: 72-99.   DOI   ScienceOn
46 Xia H, Chen L, Wang F, Lu B-R. 2010. Yield benefit and underlying cost of insect-resistance transgenic rice: implication in breeding and deploying transgenic crops. Field Crop Res 118: 215-220.   DOI   ScienceOn
47 Yang K, Jung S, Lee Y, Back K. 2006. Modifying Myxococcus xanthus protoporphyrinogen oxidase to plant codon usage and high level of oxyfluorfen resistance in transgenic rice. Pestic Biochem Phys 86: 186-194.   DOI   ScienceOn
48 Bartsch D, Brand U, Morak C, Pohl-Orf M, Schuphan I, Ell-strand NC. 2001. Biosafety of hybrids between transgenic virus-resistant sugar beet and Swiss chard. Ecol Appl 11: 142-147.   DOI   ScienceOn
49 Yoshida S, Forno DA, Cock JH, Gomez KA. 1976. Laboratory Manual for Physiological Studies of Rice, 3rd ed, The International Rice Research Institute, Los Banos, The Philippines.
50 Bartsch D, Schmidt M, Pohl-Orf M, Haag C, Schuphan I. 1996. Competitiveness of transgenic sugar beet resistant to beet necrotic yellow vein virus and potential impact on wild beet populations. Mol Ecol 5: 199-205.   DOI   ScienceOn
51 Bergelson J, Purrington CB. 1996. Surveying patterns in the cost of resistance in plants. Am Nat 148: 536-558.   DOI   ScienceOn
52 Bergelson J, Purrington CB, Palm CJ, Lopez-Gutierrez J-C. 1996. Costs of resistance: a test using transgenic Arabidopsis thaliana. P Roy Soc Lond B Bio 263: 1659-1663.   DOI   ScienceOn
53 Brandle JE, Miki BL. 1993. Agronomic performance of sulfonylurea-resistant transgenic flue-cured tobacco grown under field conditions. Crop Sci 33: 847-852.   DOI