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Existence of vigorous lineages of crop-wild hybrids in Lettuce under field conditions

Published online by Cambridge University Press:  13 August 2010

Danny A.P. Hooftman ,
Yorike Hartman ,
J. Gerard B. Oostermeijer  and
Hans (J.) C.M. Den Nijs
Danny A.P. Hooftman*
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands NERC Centre for Ecology and Hydrology, Wallingford, UK
Yorike Hartman
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
J. Gerard B. Oostermeijer
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
Hans (J.) C.M. Den Nijs
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands
*
* Corresponding author: [email protected]

Abstract

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Plant to plant gene flow is a route of environmental exposure for GM plants specifically since crosses with wild relatives could lead to the formation of more vigorous hybrids, which could increase the rate of introgression and the environmental impact. Here, we test the first step in the process of potential transgene introgression: whether hybrid vigor can be inherited to the next generation, which could lead to fixation of altered, i.e., elevated, quantitative traits.

The potential for a permanent elevated fitness was tested using individual autogamous progeny lineages of hybrids between the crop Lactuca sativa (Lettuce) and the wild species Lactuca serriola (Prickly Lettuce). We compared progeny from motherplants grown under either greenhouse or field conditions. The survival of young plants depended strongly on maternal environment. Furthermore, we observed that offspring reproductive fitness components were correlated with maternal fitness.

Our study demonstrates that post-zygotic genotypic sorting at the young plants stage reduces the number of genotypes non-randomly, leading to inheritance of high levels of reproductive traits in the surviving hybrid lineages, compared to the pure wild relatives.

Consequently, directional selection could lead to displacement of the pure wild relative and fixation of more vigorous genome segments originating from crops, stabilizing plant traits at elevated levels. Such information can be used to indentify segments which are less likely to introgress into wild relative populations as a target for transgene insertion.

Keywords

Lettucevigorous-lineagescrop-wild hybridsgene introgression
Type
Research Article
Information
Environmental Biosafety Research , Volume 8 , Issue 4 , October 2009 , pp. 203 - 217
Copyright
© ISBR, EDP Sciences, 2010

References

Andow, DA, Zwahlen, C (2006) Assessing environmental risks of transgenic plants. Ecol. Lett. 9: 196–214 CrossRefGoogle ScholarPubMed
Ayres, DR, Smith, DL, Zaremba, K, Klohr, S, Strong, DR (2004) Spread of exotic cordgrass and hybrids (Spartina sp.) in the tidal marshes of San Francisco bay, California. Biol. Invas. 6: 221–231 CrossRefGoogle Scholar
Baack, EJ, Sapir, Y, Chapman, MA, Burke, JM, Rieseberg, LH (2008) Selection on domestication traits and quantitative trait loci in crop-wild sunflower hybrids. Mol. Ecol. 17: 666–677 CrossRefGoogle ScholarPubMed
Brateler, M, Lexer, C, Widmer, A (2006) Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris . J. Evolution. Biol. 19: 1149–1156 CrossRefGoogle Scholar
Burgess, KS, Husband, BC (2006) Habitat differentiation and the ecological costs of hybridization: the effects of introduced mulberry (Morus alba) on a native congener (M. rubra). J. Ecol. 94: 1061–1069 CrossRefGoogle Scholar
Burke, JM, Arnold, ML (2001) Genetics and fitness of hybrids. Annu. Rev. Gen. 35: 31–52 CrossRefGoogle ScholarPubMed
Campbell, DR, Galen, C, Wu, CA (2005) Ecophysiology of first and second generation hybrids in a natural plant hybrid zone. Oecologia 144: 214–225 CrossRefGoogle Scholar
Campbell, DR, Waser, NM, Aldridge, G, Wu, CA (2008) Lifetime fitness in two generations of Ipomopsis hybrids. Evolution 62: 2616–2627 CrossRefGoogle ScholarPubMed
Campbell, LG, Snow, AA (2007) Competition alters life history and increases the relative fecundity of crop-wild radish hybrids (Raphanus spp.). New Phytol . 173: 648–660 CrossRefGoogle Scholar
Campbell, LG, Snow, AA, Sweeney, PM, Ketner, JM (2009) Rapid evolution in crop-weed hybrids under artificial selection for divergent life histories. Evol. Appl. 2: 172–186 CrossRefGoogle ScholarPubMed
Chandler, S, Dunwell, JM (2008) Gene flow, risk assessment and the environmental release of transgenic plants. Crit. Rev. Plant Sci. 27: 25–49 CrossRefGoogle Scholar
Charlesworth, B, Charlesworth, D, Barton, NH (2003) The effects of genetic and geographic structure on neutral variation. Annu. Rev. Ecol. Evol. 34: 99–125 CrossRefGoogle Scholar
Chapman, MA, Burke, JM (2006) Letting the gene out of the bottle: the population genetics of genetically modified crops. New Phytol. 170: 429–443 CrossRefGoogle ScholarPubMed
Chapman, MA, Pashley, CH, Wenzler, J, Hvala, J, Tang, SX, Knapp, SJ, Burke, JM (2008) A genomic scan reveals candidates for genes involved in the evolution of cultivated sunflower. Plant Cell 20: 2931–2945 CrossRefGoogle ScholarPubMed
Collard, BCY, MacKill, DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos. T. R. Soc. B . 363: 557–572 CrossRefGoogle ScholarPubMed
Collard, BCY, Jahuzer, MZZ, Brouwer, JB, Pang, ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker assisted selection for crop improvement: the basic concepts. Euphytica 142: 169–196 CrossRefGoogle Scholar
D’Andrea, L, Felber, F, Guadagnuolo, R (2008) Hybridization rates between lettuce (Lactuca sativa) and its wild relative (L. serriola) under field conditions. Environ. Biosafety Res . 7: 61–71 CrossRefGoogle ScholarPubMed
D’Andrea, L, Broennimanm, O, Kozlowski, G, Guisan, A, Morin, X, Keller-Senften, J, Felber, F (2009) Climate change, anthropogenic disturbance and the northward range expansion of Lactuca serriola (Asteraceae). J. Biogeogr. 36: 1573–1587 CrossRefGoogle Scholar
Damgaard, CJ, Jensen, BD (2002) Disease resistance in Arabidopsis thaliana increases the competitive ability and the predicted probability of long-term ecological success under disease pressure. Oikos 98: 459–466 CrossRefGoogle Scholar
Dechaine, JM, Burger, JC, Chapman, MA, Seiler, GJ, Brunick, R, Knapp, SJ, Burke, JM (2009) Fitness effects and genetic architecture of plant-herbivore interactions in sunflower crop-wild hybrids. New Phytol. 184: 828–841 CrossRefGoogle ScholarPubMed
Ellstrand NC (2003) Dangerous liaisons? When cultivated plants mate with their wild relatives. Baltimore, John Hopkins University Press
Ellstrand, NC, Schierenbeck, KA (2006) Hybridisation as stimulus for the evolution of invasiveness in plants. Euphytica 148: 35–46 CrossRefGoogle Scholar
Erickson, DL, Fenster, CB (2006) Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata . Evolution 60: 225–233 CrossRefGoogle ScholarPubMed
Galloway, LF (2005) Maternal effects provide phenotypic adaptation to local environmental conditions. New Phytol. 166: 93–99 CrossRefGoogle ScholarPubMed
Giannino, D, Nicolodi, C, Testone, G, Di Giacomo, E, Iannelli, MA, Frugis, G, Mariotti, D (2008) Pollen mediated transgene flow in lettuce (Lactuca sativa L.). Plant Breed. 127: 308–314 CrossRefGoogle Scholar
Grillo, MA, Li, CB, Fowlkes, AM, Briggeman, TM, Zhou, AL, Schemske, DW, Sang, T (2009) Genetic architecture for the adaptive origin of annual wild rice, Oryza nivara . Evolution 63: 870–883 CrossRefGoogle ScholarPubMed
Hails, RS, Morley, K (2005) Genes invading new populations: a risk assessment perspective. Trends Ecol. Evol. 20: 245–252 CrossRefGoogle ScholarPubMed
Hall, RJ, Hastings, A, Ayres, DR (2006) Explaining the explosion: modelling hybrid invasion P. Roy. Soc. B. 273: 1385–1389 CrossRefGoogle Scholar
Heffner, EL, Sorrells, ME, Jannink, JL (2009) Genomic selection for crop improvement. Crop Sci. 49: 1–12 CrossRefGoogle Scholar
Hegde, SG, Nason, JD, Clegg, JM, Ellstrand, NC (2006) The evolution of California’s wild radish has resulted in the extinction of its progenitors. Evolution 60: 1187–1197 CrossRefGoogle ScholarPubMed
Hooftman, DAP, Oostermeijer, JGB, Jacobs, MMJ, den Nijs, JCM (2005) Vital rates determine the performance advantage of crop-wild hybrids in Lettuce. J. Appl. Ecol. 42: 1086–1095 CrossRefGoogle Scholar
Hooftman, DAP, Oostermeijer, JGB, den Nijs, JCM (2006) Invasive behaviour of Lactuca serriola (Asteraceae) in The Netherlands: spatial distribution and ecological amplitude. Basic Appl. Ecol. 7: 507–519 CrossRefGoogle Scholar
Hooftman, DAP, de Jong, MJ, Oostermeijer, JGB, den Nijs, JCM (2007) Modelling the long-term consequences of crop-wild relative hybridization: a case study using four generations of hybrids. J. Appl. Ecol. 44: 1035–1045 CrossRefGoogle Scholar
Hooftman, DAP, Nieuwenhuis, BPS, Posthuma, KI, Oostermeijer, , den Nijs, JCM (2007b) Introgression potential of downy mildew resistance from lettuce to Lactuca serriola and its relevance for plant fitness. Basic Appl. Ecol. 8: 135–146 CrossRefGoogle Scholar
Hooftman, DAP, Oostermeijer, JGB, Marquard, E, den Nijs, JCM (2008) Modelling the consequences of crop-wild relative gene flow: a sensitivity analysis of the effects of outcrossing rates and hybrid vigour breakdown in Lactuca . J. Appl. Ecol. 45: 1094–1103 CrossRefGoogle Scholar
Huxel, GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol. Conserv. 89: 143–152 CrossRefGoogle Scholar
Kirk, H, Vrieling, K, Klinkhamer, PGL (2005) Maternal effects and heterosis influence the fitness of plant hybrids. New Phytol. 166: 685–694 CrossRefGoogle ScholarPubMed
Koopman, WJM, Zevenbergen, MJ, van der Berg, RG (2001) Species relationships in Lactuca s.l. (Lactuceae, Asteraceae) inferred from AFLP fingerprints. Am. J. Bot. 88: 1881–1887 CrossRefGoogle ScholarPubMed
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sunderland, Sinauer Associates, Inc.
Mercer, KL, Andow, DA, Wyse, DL, Shaw, RG (2007) Stress and domestication traits increase the relative fitness of crop-wild hybrids in sunflower. Ecol. Lett. 10: 383–393 CrossRefGoogle ScholarPubMed
Milne, RI, Abbott, RJ (2000) Origin and evolution of invasive naturalised material of Rhodendron ponticum L. in the British Isles. Mol. Ecol. 9: 541–556 CrossRefGoogle Scholar
Moles, AT, Gruber, MAM, Bonser, SP (2008) A new framework for predicting invasive plant species. J. Ecol. 96: 13–17 Google Scholar
Orozco-ter Wengel P, Sørensen A, den Nijs JCM, Hooftman DAP (2005) Hybrids between lettuce and its wild relative have an increased likelihood of carrying crop specific genome segment. Abstracts of the 90th meeting of the Ecological Society of America, Montreal
Rapp, RA, Wendel, JF (2005) Epigenetics and plant evolution. New Phytol. 168: 81–91 CrossRefGoogle ScholarPubMed
Ridley, CE, Ellstrand, NC (2009) Evolution of enhanced reproduction in the hybrid-derived invasive, California wild radish (Raphanus sativus). Biol. Invasions 11: 2251–2264 CrossRefGoogle Scholar
Rieseberg, LH, Raymond, O, Rosenthal, DM, Lai, Z, Livingstone, K, Nakazato, T, Durphy, JL, Schwarzbach, AE, Donovan, LA, Lexer, C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211–1216 CrossRefGoogle Scholar
Ryder EJ (1999) Lettuce, Endive and Chicory. Wallingford, CAB International
Snow, AA, Pilson, D, Rieseberg, LH, Paulsen, MJ, Pleskac, N, Reagon, MR, Wolf, DE, Selbo, SM (2005) A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol. Appl. 13: 279–286 CrossRefGoogle Scholar
Snow, AA, Culley, TM, Campbell, LG, Sweeney, PM, Hegde, SG, Ellstrand, NC (2010) Long-term persistence of crop alleles in weedy populations of wild radish (Raphanus raphanistrum). New Phytol. 186: 537–548 CrossRefGoogle Scholar
Stewart, CN, Halfhill, MD, Warwick, SI (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat. Rev. Genet. 4: 806–817 CrossRefGoogle ScholarPubMed
Sweet, JB (2009) The 10th International Symposium on the Biosafety of Genetically Modified Organisms (ISBGMO), Wellington, New Zealand, November 2008. Environ. Biosafety Res. 8: 161–181 CrossRefGoogle Scholar
Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (1976) Flora Europaea, vol. 4. Cambridge, Cambridge University Press
Vuilleumier, S, Yearsley, JM, Perrin, N (2008) The fixation of locally beneficial alleles in a metapopulation. Genetics 178: 467–475 CrossRefGoogle Scholar