Genetically modified crops

Humans have directly influenced the genetic makeup of plants to increase their value as a crop through domestication. The first evidence of plant domestication comes from emmer and einkorn wheat found in pre-Pottery Neolithic A villages in Southwest Asia dated about 10,500 to 10,100 BC.[29] The Fertile Crescent of Western Asia, Egypt, and India were sites of the earliest planned sowing and harvesting of plants that had previously been gathered in the wild. Independent development of agriculture occurred in northern and southern China, Africa's Sahel, New Guinea and several regions of the Americas.[30] The eight Neolithic founder crops (emmer wheat, einkorn wheat, barley, peas, lentils, bitter vetch, chick peas and flax) had all appeared by about 7,000 BC.[31] Traditional crop breeders have long introduced foreign germplasm into crops by creating novel crosses. A hybrid cereal grain was created in 1875, by crossing wheat and rye.[32] Since then traits including dwarfing genes and rust resistance have been introduced in that manner.[33] Plant tissue culture and deliberate mutations have enabled humans to alter the makeup of plant genomes.[34][35]

Modern advances in genetics have allowed humans to more directly alter plants genetics. In 1970 Hamilton Smith's lab discovered restriction enzymes that allowed DNA to be cut at specific places, enabling scientists to isolate genes from an organism's genome.[36] DNA ligases that join broken DNA together had been discovered earlier in 1967,[37] and by combining the two technologies, it was possible to "cut and paste" DNA sequences and create recombinant DNA. Plasmids, discovered in 1952,[38] became important tools for transferring information between cells and replicating DNA sequences. In 1907 a bacterium that caused plant tumors, Agrobacterium tumefaciens, was discovered and in the early 1970s the tumor inducing agent was found to be a DNA plasmid called the Ti plasmid.[39] By removing the genes in the plasmid that caused the tumor and adding in novel genes researchers were able to infect plants with A. tumefaciens and let the bacteria insert their chosen DNA sequence into the genomes of the plants.[40] As not all plant cells were susceptible to infection by A. tumefaciens other methods were developed, including electroporation, micro-injection[41] and particle bombardment with a gene gun (invented in 1987).[42][43] In the 1980s techniques were developed to introduce isolated chloroplasts back into a plant cell that had its cell wall removed. With the introduction of the gene gun in 1987 it became possible to integrate foreign genes into a chloroplast.[44] Genetic transformation has become very efficient in some model organisms. In 2008 genetically modified seeds were produced in Arabidopsis thaliana by dipping the flowers in an Agrobacterium solution.[45] In 2013 CRISPR was first used to target modification of plant genomes.[46]

The first genetically engineered crop plant was tobacco, reported in 1983.[47] It was developed creating a chimeric gene that joined an antibiotic resistant gene to the T1 plasmid from Agrobacterium. The tobacco was infected with Agrobacterium transformed with this plasmid resulting in the chimeric gene being inserted into the plant. Through tissue culture techniques a single tobacco cell was selected that contained the gene and a new plant grown from it.[48] The first field trials of genetically engineered plants occurred in France and the US in 1986, tobacco plants were engineered to be resistant to herbicides.[49] In 1987 Plant Genetic Systems, founded by Marc Van Montagu and Jeff Schell, was the first company to genetically engineer insect-resistant plants by incorporating genes that produced insecticidal proteins from Bacillus thuringiensis (Bt) into tobacco.[50] The People's Republic of China was the first country to commercialise transgenic plants, introducing a virus-resistant tobacco in 1992.[51] In 1994 Calgene attained approval to commercially release the Flavr Savr tomato, a tomato engineered to have a longer shelf life.[52] Also in 1994, the European Union approved tobacco engineered to be resistant to the herbicide bromoxynil, making it the first genetically engineered crop commercialised in Europe.[53] In 1995 Bt Potato was approved safe by the Environmental Protection Agency, after having been approved by the FDA, making it the first pesticide producing crop to be approved in the US.[54] In 1996 a total of 35 approvals had been granted to commercially grow 8 transgenic crops and one flower crop (carnation), with 8 different traits in 6 countries plus the EU.[49] By 2010, 29 countries had planted commercialised genetically modified crops and a further 31 countries had granted regulatory approval for transgenic crops to be imported.[55]

The first genetically modified animal to be commercialised was the GloFish, a Zebra fish with a fluorescent gene added that allows it to glow in the dark under ultraviolet light.[56] The first genetically modified animal to be approved for food use was AquAdvantage salmon in 2015.[57] The salmon were transformed with a growth hormone-regulating gene from a Pacific Chinook salmon and a promoter from an ocean pout enabling it to grow year-round instead of only during spring and summer.[58]

Plants (Solanum chacoense) being transformed using agrobacterium

Genetically engineered crops have genes added or removed using genetic engineering techniques,[59] originally including gene guns, electroporation, microinjection and agrobacterium. More recently, CRISPR and TALEN offered much more precise and convenient editing techniques.

Gene guns (also known as biolistics) "shoot" (direct high energy particles or radiations against[60]) target genes into plant cells. It is the most common method. DNA is bound to tiny particles of gold or tungsten which are subsequently shot into plant tissue or single plant cells under high pressure. The accelerated particles penetrate both the cell wall and membranes. The DNA separates from the metal and is integrated into plant DNA inside the nucleus. This method has been applied successfully for many cultivated crops, especially monocots like wheat or maize, for which transformation using Agrobacterium tumefaciens has been less successful.[61] The major disadvantage of this procedure is that serious damage can be done to the cellular tissue.

Agrobacterium tumefaciens-mediated transformation is another common technique. Agrobacteria are natural plant parasites.[62] Their natural ability to transfer genes provides another engineering method. To create a suitable environment for themselves, these Agrobacteria insert their genes into plant hosts, resulting in a proliferation of modified plant cells near the soil level (crown gall). The genetic information for tumor growth is encoded on a mobile, circular DNA fragment (plasmid). When Agrobacterium infects a plant, it transfers this T-DNA to a random site in the plant genome. When used in genetic engineering the bacterial T-DNA is removed from the bacterial plasmid and replaced with the desired foreign gene. The bacterium is a vector, enabling transportation of foreign genes into plants. This method works especially well for dicotyledonous plants like potatoes, tomatoes, and tobacco. Agrobacteria infection is less successful in crops like wheat and maize.

Electroporation is used when the plant tissue does not contain cell walls. In this technique, "DNA enters the plant cells through miniature pores which are temporarily caused by electric pulses."

Microinjection is used to directly inject foreign DNA into cells.[63]

Plant scientists, backed by results of modern comprehensive profiling of crop composition, point out that crops modified using GM techniques are less likely to have unintended changes than are conventionally bred crops.[64][65]

In research tobacco and Arabidopsis thaliana are the most frequently modified plants, due to well-developed transformation methods, easy propagation and well studied genomes.[66][67] They serve as model organisms for other plant species.

Introducing new genes into plants requires a promoter specific to the area where the gene is to be expressed. For instance, to express a gene only in rice grains and not in leaves, an endosperm-specific promoter is used. The codons of the gene must be optimized for the organism due to codon usage bias.

GM food's economic value to farmers is one of its major benefits, including in developing nations.[86][87][88] A 2010 study found that Bt corn provided economic benefits of $6.9 billion over the previous 14 years in five Midwestern states. The majority ($4.3 billion) accrued to farmers producing non-Bt corn. This was attributed to European corn borer populations reduced by exposure to Bt corn, leaving fewer to attack conventional corn nearby.[89][90] Agriculture economists calculated that "world surplus [increased by] $240.3 million for 1996. Of this total, the largest share (59%) went to U.S. farmers. Seed company Monsanto received the next largest share (21%), followed by US consumers (9%), the rest of the world (6%), and the germplasm supplier, Delta & Pine Land Company of Mississippi (5%)."[91]

According to the International Service for the Acquisition of Agri-biotech Applications (ISAAA), in 2014 approximately 18 million farmers grew biotech crops in 28 countries; about 94% of the farmers were resource-poor in developing countries. 53% of the global biotech crop area of 181.5 million hectares was grown in 20 developing countries.[92] PG Economics comprehensive 2012 study concluded that GM crops increased farm incomes worldwide by $14 billion in 2010, with over half this total going to farmers in developing countries.[93]

Forgoing these benefits is costly.[94][95] Wesseler et al., 2017 estimate the cost of delay for several crops including GM banana in Uganda, GM cowpea in west Africa, and GM maize/corn in Kenya.[94] They estimate Nigeria alone loses $33–46m annually.[94] The potential and alleged harms of GM crops must then be compared to these costs of delay.[94][95]

Critics challenged the claimed benefits to farmers over the prevalence of biased observers and by the absence of randomized controlled trials. The main Bt crop grown by small farmers in developing countries is cotton. A 2006 review of Bt cotton findings by agricultural economists concluded, "the overall balance sheet, though promising, is mixed. Economic returns are highly variable over years, farm type, and geographical location".[96]

In 2013 the European Academies Science Advisory Council (EASAC) asked the EU to allow the development of agricultural GM technologies to enable more sustainable agriculture, by employing fewer land, water, and nutrient resources. EASAC also criticizes the EU's "time-consuming and expensive regulatory framework" and said that the EU had fallen behind in the adoption of GM technologies.[97]

Participants in agriculture business markets include seed companies, agrochemical companies, distributors, farmers, grain elevators and universities that develop new crops/traits and whose agricultural extensions advise farmers on best practices. According to a 2012 review based on data from the late 1990s and early 2000s, much of the GM crop grown each year is used for livestock feed and increased demand for meat leads to increased demand for GM feed crops.[98] Feed grain usage as a percentage of total crop production is 70% for corn and more than 90% of oil seed meals such as soybeans. About 65 million metric tons of GM corn grains and about 70 million metric tons of soybean meals derived from GM soybean become feed.[98]

In 2014 the global value of biotech seed was US$15.7 billion; US$11.3 billion (72%) was in industrial countries and US$4.4 billion (28%) was in the developing countries.[92] In 2009, Monsanto had $7.3 billion in sales of seeds and from licensing its technology; DuPont, through its Pioneer subsidiary, was the next biggest company in that market.[99] As of 2009, the overall Roundup line of products including the GM seeds represented about 50% of Monsanto's business.[100]

Some patents on GM traits have expired, allowing the legal development of generic strains that include these traits. For example, generic glyphosate-tolerant GM soybean is now available. Another impact is that traits developed by one vendor can be added to another vendor's proprietary strains, potentially increasing product choice and competition.[101] The patent on the first type of Roundup Ready crop that Monsanto produced (soybeans) expired in 2014[102] and the first harvest of off-patent soybeans occurs in the spring of 2015.[103] Monsanto has broadly licensed the patent to other seed companies that include the glyphosate resistance trait in their seed products.[104] About 150 companies have licensed the technology,[105] including Syngenta[106] and DuPont Pioneer.[107]

In 2014, the largest review yet concluded that GM crops' effects on farming were positive. The meta-analysis considered all published English-language examinations of the agronomic and economic impacts between 1995 and March 2014 for three major GM crops: soybean, maize, and cotton. The study found that herbicide-tolerant crops have lower production costs, while for insect-resistant crops the reduced pesticide use was offset by higher seed prices, leaving overall production costs about the same.[3][108]

Yields increased 9% for herbicide tolerance and 25% for insect resistant varieties. Farmers who adopted GM crops made 69% higher profits than those who did not. The review found that GM crops help farmers in developing countries, increasing yields by 14 percentage points.[108]

The researchers considered some studies that were not peer-reviewed and a few that did not report sample sizes. They attempted to correct for publication bias, by considering sources beyond academic journals. The large data set allowed the study to control for potentially confounding variables such as fertilizer use. Separately, they concluded that the funding source did not influence study results.[108]

Under special conditions meant to reveal only genetic yield factors, many GM crops are known to actually have lower yields. This is variously due to one or both of: Yield drag, wherein the trait itself lowers yield, either by competing for synthesis feedstock or by being inserted slightly inaccurately, into the middle of a yield-relevant gene; and/or yield lag, wherein it takes some time to breed the newest yield genetics into the GM lines. This does not reflect realistic field conditions however, especially leaving out pest pressure which is often the point of the GM trait.[109] See for example Roundup Ready § Productivity claims.

Combined features of increased yield, decreased land use, reduced use of fertilizer and reduced farming machinery use create a feedback loop that reduces carbon emissions related to farming. These reductions have been estimated at 7.5% of total agricultural emissions in the EU or 33 millions tons of CO₂.[110]

Gene editing may also increase yields non-specific to the use of any biocides/pesticides. In March 2022, field test results showed CRISPR-based gene knockout of KRN2 in maize and OsKRN2 in rice increased grain yields by ~10% and ~8% without any detected negative effects.[111][112]

Genetically modified King Edward potato (right) next to King Edward which has not been genetically modified (left). Research field belonging to the Swedish University of Agricultural Sciences in 2019.

GM crops grown today, or under development, have been modified with various traits. These traits include improved shelf life, disease resistance, stress resistance, herbicide resistance, pest resistance, production of useful goods such as biofuel or drugs, and ability to absorb toxins and for use in bioremediation of pollution.

Recently, research and development has been targeted to enhancement of crops that are locally important in developing countries, such as insect-resistant cowpea for Africa[113] and insect-resistant brinjal (eggplant).[114]

The regulation of genetic engineering concerns the approaches taken by governments to assess and manage the risks associated with the development and release of genetically modified crops. There are differences in the regulation of GM crops between countries, with some of the most marked differences occurring between the US and Europe. Regulation varies in a given country depending on the intended use of each product. For example, a crop not intended for food use is generally not reviewed by authorities responsible for food safety.[219][220]

GM crops production in the World (ISAAA Brief 2019)

  More than 10 million hectares

  Between 50,000 and 10 million hectares

  Less than 50,000 hectares

  No biotech crops

In 2013, GM crops were planted in 27 countries; 19 were developing countries and 8 were developed countries. 2013 was the second year in which developing countries grew a majority (54%) of the total GM harvest. 18 million farmers grew GM crops; around 90% were small-holding farmers in developing countries.[1]

The United States Department of Agriculture (USDA) reports every year on the total area of GM crop varieties planted in the United States.[222][223] According to National Agricultural Statistics Service, the states published in these tables represent 81–86 percent of all corn planted area, 88–90 percent of all soybean planted area, and 81–93 percent of all upland cotton planted area (depending on the year).

Global estimates are produced by the International Service for the Acquisition of Agri-biotech Applications (ISAAA) and can be found in their annual reports, "Global Status of Commercialized Transgenic Crops".[1][224]

Farmers have widely adopted GM technology (see figure). Between 1996 and 2013, the total surface area of land cultivated with GM crops increased by a factor of 100, from 17,000 square kilometers (4,200,000 acres) to 1,750,000 km² (432 million acres).[1] 10% of the world's arable land was planted with GM crops in 2010.[55] As of 2011, 11 different transgenic crops were grown commercially on 395 million acres (160 million hectares) in 29 countries such as the US, Brazil, Argentina, India, Canada, China, Paraguay, Pakistan, South Africa, Uruguay, Bolivia, Australia, Philippines, Myanmar, Burkina Faso, Mexico and Spain.[55] One of the key reasons for this widespread adoption is the perceived economic benefit the technology brings to farmers. For example, the system of planting glyphosate-resistant seed and then applying glyphosate once plants emerged provided farmers with the opportunity to dramatically increase the yield from a given plot of land, since this allowed them to plant rows closer together. Without it, farmers had to plant rows far enough apart to control post-emergent weeds with mechanical tillage.[225] Likewise, using Bt seeds means that farmers do not have to purchase insecticides, and then invest time, fuel, and equipment in applying them. However critics have disputed whether yields are higher and whether chemical use is less, with GM crops. See Genetically modified food controversies article for information.

Land area used for genetically modified crops by country (1996–2009), in millions of hectares. In 2011, the land area used was 160 million hectares, or 1.6 million square kilometers.[55]

In the US, by 2014, 94% of the planted area of soybeans, 96% of cotton and 93% of corn were genetically modified varieties.[226][227][228] Genetically modified soybeans carried herbicide-tolerant traits only, but maize and cotton carried both herbicide tolerance and insect protection traits (the latter largely Bt protein).[229] These constitute "input-traits" that are aimed to financially benefit the producers, but may have indirect environmental benefits and cost benefits to consumers. The Grocery Manufacturers of America estimated in 2003 that 70–75% of all processed foods in the U.S. contained a GM ingredient.[230]

Europe grows relatively few genetically engineered crops[231] with the exception of Spain, where one fifth of maize is genetically engineered,[232] and smaller amounts in five other countries.[233] The EU had a 'de facto' ban on the approval of new GM crops, from 1999 until 2004.[234][235] GM crops are now regulated by the EU.[236] In 2015, genetically engineered crops are banned in 38 countries worldwide, 19 of them in Europe.[237][238] Developing countries grew 54 percent of genetically engineered crops in 2013.[1]

In recent years GM crops expanded rapidly in developing countries. In 2013 approximately 18 million farmers grew 54% of worldwide GM crops in developing countries.[1] 2013's largest increase was in Brazil (403,000 km² versus 368,000 km² in 2012). GM cotton began growing in India in 2002, reaching 110,000 km² in 2013.[1]

According to the 2013 ISAAA brief: "a total of 36 countries (35 + EU-28) have granted regulatory approvals for biotech crops for food and/or feed use and for environmental release or planting since 1994 ... a total of 2,833 regulatory approvals involving 27 GM crops and 336 GM events (NB: an "event" is a specific genetic modification in a specific species) have been issued by authorities, of which 1,321 are for food use (direct use or processing), 918 for feed use (direct use or processing) and 599 for environmental release or planting. Japan has the largest number (198), followed by the U.S.A. (165, not including "stacked" events), Canada (146), Mexico (131), South Korea (103), Australia (93), New Zealand (83), European Union (71 including approvals that have expired or under renewal process), Philippines (68), Taiwan (65), Colombia (59), China (55) and South Africa (52). Maize has the largest number (130 events in 27 countries), followed by cotton (49 events in 22 countries), potato (31 events in 10 countries), canola (30 events in 12 countries) and soybean (27 events in 26 countries).[1]

Direct genetic engineering has been controversial since its introduction. Most, but not all of the controversies are over GM foods rather than crops per se. GM foods are the subject of protests, vandalism, referendums, legislation, court action[239] and scientific disputes. The controversies involve consumers, biotechnology companies, governmental regulators, non-governmental organizations and scientists.

Opponents have objected to GM crops on multiple grounds including environmental impacts, food safety, whether GM crops are needed to address food needs, whether they are sufficiently accessible to farmers in developing countries,[28] concerns over subjecting crops to intellectual property law, and on religious grounds.[240] Secondary issues include labeling, the behavior of government regulators, the effects of pesticide use and pesticide tolerance.

A significant environmental concern about using genetically modified crops is possible cross-breeding with related crops, giving them advantages over naturally occurring varieties. One example is a glyphosate-resistant rice crop that crossbreeds with a weedy relative, giving the weed a competitive advantage. The transgenic hybrid had higher rates of photosynthesis, more shoots and flowers, and more seeds than the non-transgenic hybrids.[241] This demonstrates the possibility of ecosystem damage by GM crop usage.

There is a scientific consensus[8][9][10][11] that currently available food derived from GM crops poses no greater risk to human health than conventional food,[12][13][14][15][16] but that each GM food needs to be tested on a case-by-case basis before introduction.[17][18][19] Nonetheless, members of the public are much less likely than scientists to perceive GM foods as safe.[20][21][22][23] The legal and regulatory status of GM foods varies by country, with some nations banning or restricting them, and others permitting them with widely differing degrees of regulation.[24][25][26][27]

No reports of ill effects from GM food have been documented in the human population.[242][243][244] GM crop labeling is required in many countries, although the United States Food and Drug Administration does not, nor does it distinguish between approved GM and non-GM foods.[245] The United States enacted a law that requires labeling regulations to be issued by July 2018. It allows indirect disclosure such as with a phone number, bar code, or web site.[246]

Advocacy groups such as Center for Food Safety, Union of Concerned Scientists, Greenpeace and the World Wildlife Fund claim that risks related to GM food have not been adequately examined and managed, that GM crops are not sufficiently tested and should be labelled, and that regulatory authorities and scientific bodies are too closely tied to industry. Some studies have claimed that genetically modified crops can cause harm;[247][248] a 2016 review that reanalyzed the data from six of these studies found that their statistical methodologies were flawed and did not demonstrate harm, and said that conclusions about GM crop safety should be drawn from "the totality of the evidence ... instead of far-fetched evidence from single studies".[249]

• "EU Register of authorised GM crops".
• "Biotechnology Consultations on Food from GE Plant Varieties".
• "Current & Previously Registered Section 3 PIP Registrations".