Direct and reverse pollen-mediated gene flow between GM rice and red rice weed

Research Article Direct and reverse pollen-mediated gene flow between GM rice and red rice weed X. Serrat1*†, R. Esteban 1†, G. Peñas1, M. M. Català 2, E. Melé 1 and J. Messeguer 1 1 IRTA, Center for Research in Agricultural Genomics (CSIC-IRTA-UAB-UB), Campus UAB, Edifici CRAG, Bellaterra (Cerdanyola del Vallès), E-08193 Bellaterra, Spain 2 IRTA Ctra. Balada km. 1, 43 870 Amposta, Spain Received: 19 June 2013; Accepted: 24 October 2013; Published: 7 November 2013 Citation: Serrat X, Esteban R, Peñas G, Català MM, Melé E, Messeguer J. 2013. Direct and reverse pollen-mediated gene flow between GM rice and red rice weed. AoB PLANTS 5: plt050; doi:10.1093/aobpla/plt050 Abstract. Potential risks of genetically modified (GM) crops must be identified before their commercialization, as happens with all new technologies. One of the major concerns is the proper risk assessment of adventitious presence of transgenic material in rice fields due to cross-pollination. Several studies have been conducted in order to quantify pollen-mediated gene flow from transgenic rice (Oryza sativa) to both conventional rice and red rice weed (O. sativa f. spontanea) under field conditions. Some of these studies reported GM pollen-donor rice transferring GM traits to red rice. However, gene flow also occurs in the opposite direction, in a phenomenon that we have called reverse gene flow, resulting in transgenic seeds that have incorporated the traits of wild red rice. We quantified reverse gene flow using material from two field trials. A molecular analysis based on amplified fragment length polymorphisms was carried out, being complemented with a phenotypic identification of red rice traits. In both field trials, the reverse gene flow detected was greater than the direct gene flow. The rate of direct gene flow varied according to the relative proportions of the donor (GM rice) and receptor (red rice) plants and was influenced by wind direction. The ecological impact of reverse gene flow is limited in comparison with that of direct gene flow because non-shattered and nondormant seeds would be obtained in the first generation. Hybrid seed would remain in the spike and therefore most of it would be removed during harvesting. Nevertheless, this phenomenon must be considered in fields used for elite seed production and in developing countries where farmers often keep some seed for planting the following year. In these cases, there is a higher risk of GM red rice weed infestation increasing from year to year and therefore a proper monitoring plan needs to be established. Keywords: Field trial; gene flow; herbicide resistance; Oryza sativa; red rice; risk assessment; transgenic rice. Introduction Genetic modification technologies are widely used as a way to introduce new genetic traits into crops of interest. One of the main environmental concerns about these technologies is the non-controlled gene spread between crops at different levels. There are many studies studying this phenomenon and reporting guidelines to minimize the risk of cross-pollination between modified plants and non-modified crop plants (Mallory-Smith and Zapiola 2008; Devos et al. 2009). These studies propose solutions like the use of different crop species working as a natural barrier against cross-pollination, minimum distances * Corresponding author’s e-mail address: † These two authors contributed equally to this work. Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2013 1 Serrat et al. — Pollen-mediated gene flow between GM rice and red rice weed between crop fields or a delay in flowering coincidence. However, all those gene flow studies are focused on the risk of the genetically modified (GM) pollen spreading out towards the non-modified crops or to the wild species that surround the fields. In our study, the influence of weedy red rice (Oryza sativa f. spontanea) gene flow over a GM rice line (O. sativa) was studied in the north-east of Spain, under Mediterranean climate conditions. The gene flow from a GM rice line to the weedy rice was also quantified in order to be able to compare both types of gene flow. Weedy rice is one of the most notorious weeds found in rice-growing areas throughout the world. It can be defined as any spontaneously and strongly shattered rice that occurs in cultivated rice fields (Xia et al. 2011). Red rice is a conspecific weedy relative of cultivated rice that has been hybridized recurrently, increasing its genetic diversity as well as its adaptability to different rice cultural environments (Langevin et al. 1990). Although it is mainly self-pollinated, it can produce viable and fertile hybrids that exhibit the dominant traits of the parental weed (Langevin et al. 1990; Noldin et al. 1999; Gealy et al. 2002, 2003). It is characterized by superior competitive ability (Diarra et al. 1985; Burgos et al. 2006), protracted flowering and seed maturation, high shattering, varying degrees of dormancy (Cohn and Hughes 1981) and a red pericarp. When red rice is mixed with cultivated rice grains at harvest, it reduces the quality of the white rice grain (Ottis et al. 2005). This constitutes an important economic problem for rice farmers given the major impact that this has on the yield and quality of harvested rice. Crop rotation is the best method for controlling weeds, while spraying herbicides has only a limited effect on the control of red rice weed. However, when crop rotations are not possible, false seeding and puddling may also provide a degree of control (Català 1995; Messeguer et al. 2004). According to United Nations’ estimates, the world population will grow from 6 billion in 2000 to 8 billion in 2025. The relationship between the growth in the world’s population and grain production has shifted over the last halfcentury, with it being possible to divide this period into two distinct sub-periods. From 1960 to 1985, the growth in grain production easily exceeded that of population, with per capita harvests increasing from 279 kg in 1960 to 343 kg in 1985. However, during the following 15 years, the growth in grain production fell behind that of population growth, mainly due to a slower growth in the use of irrigation and fertilization (Khush 2005). Global environmental degradation, in the form of salinization, pollution and global warming (Peng et al. 2004), has also reduced the availability of suitable arable land and water. All of these effects, combined with the high cost of energy-dependent 2 labour and fertilizers and phytosanitary treatments and their environmental impact, have contributed to the need to pr (...truncated)