Spontaneous gene flow is known to occur among domesticated, weedy, and wild rice plants, as in many other crop – wild relative systems . Therefore, in this article, we use the case of cultivated rice and weedy rice in China to address this topic. We first describe the cultivated rice – weedy rice study system in China. We then present the current state of development of GE cultivated rice for commercialization in China with emphasis on the two traits most likely to be first deregulated: insect resistance and herbicide tolerance. We follow with a review of the research that has been conducted to address the following questions: What is the likelihood of gene flow from cultivated rice to weedy rice? How does a transgene change the fitness of crop-weed rice hybrid populations? Finally, we compare the results from rice studies in China with a brief review of a few other systems. Based on these results, we conclude with some of the generalities that have already emerged.Weedy rice, also referred to as “red rice”, is a noxious weed , extensively infesting rice fields, particularly in Asia, the Americas, Africa, and southern Europe . Compared to cultivated rice, weedy rice has the following characteristics that contribute to its success as a weed: earlier maturity, drying rack for weed considerable seed shattering; greater seed persistence in the seed bank; more robust plant growth, increased reproductive ability; and greater genetic diversity and phenotypic plasticity .
A centuries-old problem in rice-growing areas, weedy rice has recently re-emerged as a problem where direct seedling of cultivated rice has replaced transplanting and less weed control is available . The presence of weedy rice in cultivated rice fields can cause substantial crop yield losses, varying from 5 to 100%, depending on the weed’s density in the field . Likewise, when its seeds are coharvested with those of the crop, the result is reduced grain quality . Sometimes, the weed grows so densely that farmers are forced to abandon their rice fields . Thus, weedy rice has become a major threat to rice production and world food security. The origin and evolution of weedy rice is associated with the domestication of rice, as is the case of the weedy relatives of many other crops . Research has revealed that four different evolutionary pathways result in what we call weedy rice sensulato . First, some populations of weedy rice have directly evolved from wild rice species that grow in habitats that do not depend on human disturbance . These wild taxa not only occur as weeds of rice but also as weeds for some other crops . The remaining three pathways result in weedy rice that is restricted to rice fields and their immediate vicinity. Some other weedy rice populations have evolved from natural hybrids between cultivated rice and their reproductively compatible wild relatives , Vaughan et al. 2001; Londo and Schaal 2007. The preceding two pathways involve wild progenitors.
Therefore, for these populations, the traits associated with weediness, such as seed dormancy, can be traced back to the wild ancestors. The third pathway involves hybridization between distantly related rice varieties, such as indica and japonica, with subsequent recombination. A recent study suggested that the application of hybrid rice may also result in the origin and evolution of some weedy rice populations in China . The final pathway, dedomestication, involves the loss of domestication traits in cultivated rice due to mutation, although not necessarily due to back mutation , the second type of direct evolution of some weedy rice lines from cultivated rice . The latter two evolutionary pathways to weedy rice only involve cultivated progenitors. As a consequence, the genomic constitution of these types of weedy rice is almost exclusively from the crop, with the evolution of a few novel traits not present in the cultivated lines such as red/brown pericarps and temperature-regulated seed germination, which compensates for the absence of seed dormancy . Broad definitions of weedy rice involve “plants of the genus Oryza that infest and compete with rice and other crops” including plants of wild rice species in the genus Oryza. The definition conflates the conspecific weed of human-managed habitats with wild species that can live and reproduce in both natural and managed habitats. In this article, focus on weedy rice sensustricto, employing Wang et al.’s definition of weedy rice: “rice plants with strong seed shattering and weediness that only occur inside and in the vicinity of rice fields, and can only reproduce in the human-disturbed environment.”
This definition includes only the three weedy rice lineages that are descended fully or in part from cultivated rice. Thus, weedy rice sensu stricto is Oryza sativa f. spontanea, a free-living plant that is conspecific with cultivated rice . The traits of weedy rice relative to its crop ancestor enumerated above enable it reproduce and persist in rice fields for years. The close evolutionary relationship of weedy rice with its cultivated and wild progenitors results in sporadic multi-way gene flow in sympatry or peripatry . Thus, weedy rice populations are often evolutionarily dynamic. They can accumulate genetic diversity as a potential substrate for rapid adaptive evolution. Indeed, studies have shown that weedy rice populations across the world possess abundant phenotypic and genetic diversity . At one extreme, entire weedy rice populations look superficially similar to wild species or, at the other extreme, nearly identical to cultivars. In general, weedy rice populations vary continuously between the wild and cultivated rice species for their morphological and genetic traits , with most weedy rice populations phenotypically favoring their cultivated progenitor. This trend reflects the adaptive evolution of weedy rice in human-managed agricultural environments. Pre-existing variation and that provided by gene flow has enabled the evolution of crop mimicry; that is, weedy rice typically mimics the phenotypic and physiological characters of its locally co-occurring rice cultivars. Crop mimicry is an evolutionary response to selection under farmers’ visually guided hand weeding . Obviously, the evolution of mimicry can be promoted by gene flow and introgression from sympatric cultivated rice . Collectively, crop mimicry and its other characteristics make weedy rice extremely difficult to control once it establishes in a rice field. Crop-to-weed gene flow could provide other traits that might benefit weedy rice populations. In the case of recently improved rice varieties, both transgenic and nontransgenic, these traits include, for example, insect resistance, herbicide tolerance, disease resistance, drought tolerance, salt tolerance, and cold tolerance. As crop gene flow introduces traits into weedy rice populations, the weed can evolve quickly to adapt to the changing crop management practices, such as the shift from seedling transplantation to direct seedling and that from manual and mechanical weeding to weed control by herbicides . For example, the Clear field herbicide-tolerant rice variety, a product of “mutation breeding” is grown in USA, South and Central Americas, southern Europe, and Southeast Asia . The herbicide/variety system has been successful for weed control in some countries for a short time. But in others, the combination of introgression of the tolerance gene into weedy rice populations and strong selection by the herbicide has rapidly negated the utility of the herbicide/variety weed management system, with severely reduced yields for the farmers using the system . What is the future for the evolution of weedy rice under gene flow from GE rice? Whether or not an introgressed transgene will have similar negative consequences will depend on largely four factors: the intended expressed transgene phenotype; the typical gene flow rates from the crop to the weed; the phenotype of weed with an introgressed transgene in terms of their ability to reproduce and increase relative to the nonintrogressed weed; and the introgressed weed’s relative ability to reduce the yield of their sympatric crop cultivar.
To address these factors, we examine the state of the art in China, is the primary site of GE rice development, for the various intended GE phenotypes being field released and in line for commercialization.China has invested substantially on developing biotechnology , including the creation of GE crops. Consequently, a large number of crop varieties/lines with diverse transgenic traits have been produced, pipp mobile storage systems some of which have entered commercial production . As one of the three most important national crops , rice is a priority for genetic engineering in China . During the last two decades, a large number of GE rice lines with diverse transgenic traits have been developed . Insect-resistant and herbicide-tolerant GE rice lines are prioritized transgenic traits because of the tremendous yield losses caused by insect and weed pests in China’s major rice-growing regions. The commercialization of insect-resistant cotton in China has effectively controlled cotton’s major target insect pest, cotton bollworm . The success has encouraged scientists developing insect-resistant rice . Many GE rice lines have been developed to reduce damage from its primary insect pests , especially the chewing lepidopterans and sucking hemipterans . An important milestone for GE rice was when the Ministry of Agriculture of China, authorized by the National Biosafety Committee for Genetically Engineered Organisms, issued two biosafety certificates to two Bt rice lines: Huahui-1 and Bt-Shanyou-63 in 2009, after nearly 15 years of assessment for food safety and environmental safety . In addition, five other GE lines were also approved for field experiments, including Kemingdao , T1c-9 , T2A-1 , and Kefeng-6 and Kefeng-8 . The bio-safety certificates for Huahui-1 and Bt-Shanyou-63 that were expired in 2014 were renewed by the MOA of China in 2015 for five more years. Chinese rice breeders have produced additional insect-resistant rice lines by hybridization and back-crossing between Huahui-1 and various improved rice varieties.The development of herbicide-tolerant GE rice in China has also developed rapidly in the last two decades, motivated by China’s recent shift from manual or mechanical weed management to chemical control. As direct seedling rapidly replaces seedling transplantation, highly efficient herbicide-tolerant GE rice lines are expected to reduce rice production costs. The first herbicide GE rice line containing a Bar transgene was developed by the China National Rice Research Institute in the early 1990s . The Bar transgene allows the crop to tolerate the herbicide phosphinothricin . The transgene expresses the enzyme phosphinothricin-Acetyl transferase which converts PPT into a nonphytotoxic metabolite. Shortly thereafter, various glyphosate tolerant GE rice lines were developed by transformation with microbial transgenes . Chinese scientists also developed new types of herbicide-tolerant transgenes with substantially increased 5-enolpyruvoylshikimate-3-phosphate synthase expression by adding the strong ubiquitin promotor from maize, or/and the induced mutation epsps 102 created via the error-prone polymerase chain reaction . The modified epsps transgenes were introduced into a widely used rice variety Minghui-86 via Agrobacterium transformation, generating the glyphosate tolerant GE rice line . In the recent years, GE rice lines have been produced with multiple traits. Transgene stacking can be achieved by various methods such as cotransformation with different transgenes, hybridization between GE lines with different transgenic events, linked transgenes or multigene cassette transformation, and retransformation . Many wellknown GE rice products such as Golden Rice contain stacked transgenes. In China, some GE lines containing different stacked insect-resistance transgenes have been developed to confer wider and stronger resistance to the target insects ; other GE rice lines contain a stacked combination of insect-resistance transgenes with those for other purposes . By the end of 2010, more than 170 GE rice lines created in China had entered bio-safety assessment trials authorized by Chinese government . None has yet entered commercial production. Undoubtedly, some GE rice varieties will eventually enter commercial production after the required safety assessments are completed. In particular, a primary source of pressure is some Chinese rice farmers who are enthusiastic about adopting insect-resistant transgenic rice . Nonetheless, transgene flow from GE rice to coexisting weedy rice and its consequences remain a concern – and a potential constraint – for the commercialization of GE rice. Therefore, we next examine what is known about gene flow from cultivated rice to its conspecific weed.Spontaneous pollen-mediated gene flow between domesticated crops and spatially adjacent wild/weedy taxa is not uncommon . With GE crops growing in field tests and under millions of hectares of commercial cultivation in dozens of countries worldwide, questions of the opportunities for and consequences of transgene flow to wild/weedy have received increasing discussion .