Genetic Engineering of Rice

Contribution to Sustainable Agriculture?

(a contribution to the 3rd meeting of the BSWG, 13-17 October 1997, Montreal)

by Hartmut Meyer & Karin Reiter
Working Group on Biodiversity
Forum for Environment and Development, Germany

1 Introduction

Sustainability has become a key term in the international debate since the Earth Summit (UNCED) in Rio. Hopes were created by the advocates of modern biotechnology that this technology will greatly reduce the use of chemical herbicides and pesticides and thus lower the negative impact of intensive farming on the environment as well as on human and animal health. This article evaluates research done on crops genetically engineered to be resistant to herbicides or pests and points at the hazards linked to this approach. The article especially focuses on rice, a major crop of the developing countries.

2 State of science

Major efforts in genetic engineering crop plant are currently focussed on plants and rural systems of the Northern hemisphere. The most research on important crops of developing countries has been performed with rice (HAVUKKALA 1996). Development is most advanced in genetically engineering two traits: herbicide- resistance (DATTA et al. 1992; LI et al. 1992) and Bt-toxin production (FUJIMOTO et al. 1993).

3 Problems of chemical weed control in rice

Weed problems in rice are closely correlated to the degree of production intensity. Rice production systems of Asian countries have changed dramatically (OLAFSDOTTER et al. 1996) in recent years. Increasing wealth and wages in non-agricultural sectors lead to a migration of laborers from rural regions. Herbicides could substitute for manual weed control as they became relatively cheaper. The replacement of planting technology in water by direct sowing on dry ground gave weeds more possibilities for germination and growth. The use of herbicides and efforts to control partially resistant monocotyledonous weeds (grasses) manually led to selection of weeds that are hardly distinguishable from rice (BARRET 1983). Furthermore the use of mineral fertilisers paired with semi-dwarf rice varieties increases the relative competitiveness of certain weeds. Today, Oryza rufipogon (Wild or Red Rice) and Echinochloa crus-galli are causing severe weed problems (NAYLOR 1994, HEONG et al. 1995). Despite herbicide use, weeds account for greater losses in modern than in-traditional rice production systems (NAYLOR 1994). It is against such a background that genetic engineering of herbicide resistant rice was attempted. Recent deliberate releases of glufosinate-resistant varieties in the US were conducted in order to control Red Rice (BRAVERMAN & LINSCOMBE 1994, SANKULA et al. 1997)

3.1 Herbicide resistant rice

The introduction of herbicide resistant plants in developing countries is a controversial issue. An increasing and excessive dependence on chemicals is predicted. According to the chemical industry the advantages of herbicide resistance are as follows:

  • simplification of weed control by killing higher proportions of target pests
  • substitution of environmentally damaging with environmentally friendly herbicides
  • elimination of the phytotoxic effects of herbicides in resistant crop plants
  • reduction of the amounts of herbicides applied
  • reduction of the costs of weed control

The reasons given can only be deemed as advantages if large scale, industrial type production is chosen as reference. If we compare herbicide resistant rice systems with the traditional or modern organic farming practices, this new technology does not lead to an improvement with regard to the protection of resources. (BRAY (1997) showed that the industrial systems of rice production are not sustainable in comparison to traditional ones, these unsustainable characteristics will not be changed by the introduction of herbicide resistant rice. Recent research shows that herbicide resistant rice is likely to be introduced within the Liberty Link system of AgrEvo. The new glufosinate-containing herbicide used with transgenic rice will be sold under the trade name Liberty, the older and well-known glufosinate-based herbicide Basta will be still on the market for unselective use. It has to be pointed out that Basta is registered as toxic for fish and fish feed in Germany. In many regions of South-East Asia such a toxicity would have a major socioeconomic impact with regard to integrated fish-rice production systems. Basta is highly toxic to larvae of two tested insect species on which fish feed (BASTIAN 1987). At least in Germany, Liberty will contain the same chemical formulation as Basta (GLAYMEYER, AgrEvo Germany, pers. comm.). Whether the amounts of herbicide applied or the costs will decline in practice has to be proven yet. Field trials in Germany show that Liberty does not kill all weeds and has to be supplemented with conventional herbicides (RESCHKE 1996). It is well known that the German Federal Agency for Plant Varieties does not recognize any cost reduction for farmers using glufosinate resistant rape seed and corn. The approval of these Liberty Link systems as variety under the current law is highly questionable. Even in the case of cost intensive sugar beets, the advantages of the Liberty Link system is debatable (MARLANDER 1996).

3.2 Stability of the system Herbicide Resistant Crops

A long term use of herbicide resistant crops can only be ensured if weeds do not develop resistance as well. Two factors have to be considered: the frequency at which resistance arises and the speed with which resistance spreads.

The evolution of herbicide resistance in weeds by herbicide selection is well known. Resistances directed against triazine herbicides occured 15 years after the introduction of triazines and can be found in more than 100 plant species now (JASENIUK et al. 1996). The speed with which resistance genes spread depends on the gene's location in the genome of the plant. Triazines inhibit a photosynthetic protein encoded by a gene located in the choloroplast's genome. A mutation in this gene cannot be transferred to other plants by pollen because pollen does not contain chloroplasts. The only way of spreading these mutations is by seed dispersal which results in a rather slow rate of spreading. Examples of a faster spread are found for resistances to nine other herbicides which are due to mutations in nuclear genes (JASENIUK 1996) and can therefore produce resistant offspring by pollination. After five years of use of Besulfuron (sulfonylurea herbicide) in Californian rice production, four resistant weeds appeared (PAPPAS- FADER et al. 1994). In other regions of the US such plants could be found after only three years (GUTTIERI et al. 1996).

These resistances are caused by spontanous mutations. Transgenic herbicide resistant plants will create a new type of resistance as with these plants resistance genes are brought into the agro- ecosystem intentionally in vast numbers. If there are weeds which can be pollinated by transgenic pollen and produce fertile hybrids, a strong resistance gene flow into the weed population can be predicted. In the case of rape seed this new possibility of creating herbicide resistant weeds in agro-ecosystems of Europe and North America has been described recently (JORGENSON & ANDERSEN 1994; BROWN & BROWN 1996; MIKKELSEN et al. 1996). Because the transgenes are positioned in the plant nuclei a rapid spread of resistant weeds similar to that described above for sulfonylurea resistant weeds can be expected.

In the case of herbicide resistant rice, our hypothesis is that at least one resistant weed will occur promptly: the Wild Rice. Wild Rice crosses with cultured rice (HARLAN et al. 1973). Already OKA and CHANG (1959) detected characteristics of cultured rice in populations of Wild Rice. According to KIANG et al. (1979) the initial event in the process leading to the extinction of Wild Rice in Taiwan was the gene flow from Japonica varieties introduced in the 1930s. An experiment carried out in the greenhouse failed to detect such a gene flow (KIMURA et al. 1992). However, in view of the gene flow which has been found repeatedly between transgenic rape seed and weed relatives, that single experiment cannot be the basis for a sound risk assessment. Consequently, OLAFSDOTTER et al. (1996) asked for a appropriate research before introducing transgenic herbicide resistant rice into the market.

3.3 Herbicide resistance in rice as feature of a sustainable agriculture

The use of transgenic herbicide resistant rice will lead to development of resistant Wild Rice within a few years, thus offering no improvement to the present situation. The problems weeds pose to intensive rice production over a medium or long time scale remain unsolved.

4 Problems of chemical insect control in rice

Despite the intensive use of synthetic insecticides, insects still cause serious losses in rice production. According to HEONG et al. (1995) this is not due to insufficient toxicity of the insecticides, but to unsufficient knowledge and education of the farmers with regard to the complex functions of agroecosystems. In contrast to the chemical insect control integrated and organic pest management systems rely on a number of different approaches. These are for example the use of biological insecticides like Bt proteins and breeding of resistant varieties. In the case of rice, such breeding had been successful in several cases but failed in breeding resistance towards larvae of Scirpophaga incertulans, a major pest in high input rice production (HERDT 1991).

4.1 Genetically engineered "insect resistant" rice

The introduction of Bt genes into rice is discussed as a solution to the problems with S. incertulans (ESTRUCH et al. 1997; NAYAK et al. 1997) and is seen as a contribution to integrated pest management. The often used term "insect resistant" plants is misleading because genetically engineered plants with Bt genes are produced to be toxic for one or a few insect species. Plant pathogenic insects from groups like grashoppers, aphids, and some beetles are not susceptible to the Bt toxins. While herbicide resistance works via the resistance of the plant towards a new herbicide and therefore fixes the use of chemical production factors "insect resistant" plants produce their own insecticides. Manufacturers claim that the cropping of Bt plants will lead to a significant reduction or even elimination of synthetical insecticides in intensive agriculture. If this will be true with such highly selective plants is questionable. In intensive agricultural systems, insecticides will still be used in order to control pathogenic insects which are not susceptible to Bt. Furthermore it has to be clear that Bt plants are only of value to farmers as long as no cheaper means of insect control are on the market. The main reason for planting Bt crops is an anticipated cost advantage and not the reduction of environmental impacts. In the US the planned market introduction of the insecticide Tracer by Dow Elanco may outcompete the claimed cost advantage of Bt plants (RISSLER 1997). As long as the environmental costs of high input agriculture can be externalized a sustainable development in agriculture is hindered.

4.2 Stability of the system Bt Producing Crops

The long term use of Bt plants depends on the absence of insects which developed resistances. The use of Bt proteins as natural insecticides has been seen as sustainable in the past. Most experts were of the opinion that insects will not develop resistances against these natural toxins (LUTHY et al. 1985). Since now, only one insect species (Plutella xylostella) developed resistance towards natural Bt products (McGAUGHEY 1985; TABASHNIK 1994). As reviewed by TAPPESER (1997) the genetically engineered Bt genes and toxins in crop plants dilfer from their natural occuring counterparts in microorganisms. The continous presence of partially cleaved Bt toxins in transgenic plants will lead to a strong selection pressure on pathogenic insects and therefore cannot been seen as a technological advance in comparision to the current use of Bt in integrated or organic systems.

The need for an efficient anti-resistance management shemes together with the market introduction of Bt-plants is obvious. To illustrate the problems which Bt expressing plants can cause in agriculture, the experience with Bt cotton serves as an example. In the course of the registration of transgenic Bt cotton seed, the Australian regulatory agencies did not see enough scienfific evidence to create such a management system (FORRESTER & BIRD 1996). Based on the same state of science, the US regulatory agencies developed a management system to slow down the rate of resistance development (MATTEN et al. 1996) with following features:

  • homogenously high Bt content in all parts of the transgenic plants to kill nearly 100% of target insects
  • creation of refuges of non-transgenic plants to maintain sufficiently large populations of non-resistant insects
  • use of several Bt-genes to eliminate insects which developed resistance towards one Bt-toxin

The US concept relies on following asssumptions:

  • the high and uniform Bt content transgenic which plants exhibit in the laboratory will be stable under field conditions and throughout the entire life cyclus of the plant
  • Bt resistance genes in insects will be inherited recessively, a crossing of resistant insects with non-resistant from the refuges will dilute the number of resistant individuals in the population
  • resistance genes are rare, multiple resistances will occur at an even lower rate

The validity of these assumptions is crucial for the quality of the proposed management system. According to the experiences with the first Bt cotton planted in the US and Australia and the results of new scientific research, the validity of the assumptions has been thrown in doubt. Significant losses due to unexpecting high insect infections occured during the first cropping season (FOX 1996; KAISER 1996; MACILWAIN 1996; FOX 1997). According to Monsanto a unexpectedly high pathogen pressure caused these losses.

Based on reports that the lower parts of the plants have been damaged more seriously than the upper parts, BENBROOK and HANSEN came to the conclusion that the Bt content of the cotton plants was not high enough in all plant tissues. Transgenic Bt rice developed so far does not fulfill the first feature of risk management. According to FUJIMOTO et al. (1993) losses by Chilo suppressalis and Cnaphalocrocus medinalis were reduced only by 50% and 45%, respectively. Recently developed plants showed a 86% protection towards S. incertulans (NAYAK et al. 1997). The supposed rarety of resistance genes and the lack of multiple resistences have been falsified by IQBAL et al. (1996), GOULD et al. (1997) and TABASHNIK et al. (1997). IQBAL et al. (1996) described multiple resistances in natural populations of P. xylostella of in Malaysia, while GOULD et al. (1997) showed that resistance genes are present in natural populations of Heliothis virescens in unexpected high numbers. TABASHNIK et al. (1997) demonstrated that members of populations of P. xylostella which had not been in contact with insecticides for a 100 generations carried a multiple resistance gene to four related Bt toxins in high frequencies. The development of Bt resistant insects will be accelerated by the use of Bt plants. These effects of genetically modified plants will threaten existing practices of sustainable agriculture by eliminating the possibility of using Bt-preparations as natural non-toxic insecticides in integrated and organic farming practices. Being aware of this threat, 50 agricultural organisations from the Phillipines have called for a ban of Bt rice (DOETZKIES 1997).

4.3 Bt rice as feature of a sustainable agriculture

According to ROUSH (1994) the use of Bt plants will lead to a short term reduction of insecticides. It is very likely that the use of Bt plants will cause a massive development of resistant insects. To fight these insects, farmers will have to return to the full use of synthetic insecticides after this initial period. Furthermore, Bt toxins will loose their effectiveness and the ongoing development of sustainable cropping systems will loose the most enviromnentally and toxicologically friendly pesticide which is on the market. Agenda 21 has declared, that the use of synthetical insecticides is non-sustainable according to the experience of the past 50 years. A similar characterization of Bt plants can already be made before the introduction to the market.

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