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Genetically modified crops (GM crops) are plants used in agriculture, the DNA of which has been modified using genetic engineering methods. Plant genomes can be engineered by physical methods or by use of Agrobacterium for the delivery of sequences hosted in T-DNA binary vectors. In most cases, the aim is to introduce a new trait to the plant which does not occur naturally in the species. Examples in food crops include resistance to certain pests, diseases, environmental conditions, reduction of spoilage, resistance to chemical treatments (e.g. resistance to a herbicide), or improving the nutrient profile of the crop. Examples in non-food crops include production of pharmaceutical agents, biofuels, and other industrially useful goods, as well as for bioremediation.^[1]

Farmers have widely adopted GM technology. Acreage increased from 1.7 million hectares in 1996 to 185.1 million hectares in 2016, some 12% of global cropland. As of 2016, major crop (soybean, maize, canola and cotton) traits consist of herbicide tolerance (95.9 million hectares) insect resistance (25.2 million hectares), or both (58.5 million hectares). In 2015, 53.6 million ha of Genetically modified maize were under cultivation (almost 1/3 of the maize crop). GM maize outperformed its predecessors: yield was 5.6 to 24.5% higher with less mycotoxins (−28.8%), fumonisin (−30.6%) and thricotecens (−36.5%). Non-target organisms were unaffected, except for lower populations some parasitoid wasps due to decreased populations of their pest host European corn borer; European corn borer is a target of Lepidoptera active Bt maize. Biogeochemical parameters such as lignin content did not vary, while biomass decomposition was higher.^[2]

A 2014 meta-analysis concluded that GM technology adoption had reduced chemical pesticide use by 37%, increased crop yields by 22%, and increased farmer profits by 68%.^[3] This reduction in pesticide use has been ecologically beneficial, but benefits may be reduced by overuse.^[4] Yield gains and pesticide reductions are larger for insect-resistant crops than for herbicide-tolerant crops.^[5] Yield and profit gains are higher in developing countries than in developed countries.^[3] Pesticide poisonings were reduced by 2.4 to 9 million cases per year in India alone.^[6] A 2011 review of the relationship between Bt cotton adoption and farmer suicides in India found that "Available data show no evidence of a 'resurgence' of farmer suicides" and that "Bt cotton technology has been very effective overall in India."^[7] During the time period of Bt cotton introduction in India, farmer suicides instead declined by 25%.^[6]

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]}

History

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.^[28] 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.^[29] 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.^[30] 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.^[31] Since then traits including dwarfing genes and rust resistance have been introduced in that manner.^[32] Plant tissue culture and deliberate mutations have enabled humans to alter the makeup of plant genomes.^[33][34]

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.^[35] DNA ligases that join broken DNA together had been discovered earlier in 1967,^[36] and by combining the two technologies, it was possible to "cut and paste" DNA sequences and create recombinant DNA. Plasmids, discovered in 1952,^[37] 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.^[38] 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.^[39] As not all plant cells were susceptible to infection by A. tumefaciens other methods were developed, including electroporation, micro-injection^[40] and particle bombardment with a gene gun (invented in 1987).^[41][42] 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.^[43] 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.^[44] In 2013 CRISPR was first used to target modification of plant genomes.^[45]

The first genetically engineered crop plant was tobacco, reported in 1983.^[46] 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.^[47] 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.^[48] 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.^[49] The People's Republic of China was the first country to commercialise transgenic plants, introducing a virus-resistant tobacco in 1992.^[50] In 1994 Calgene attained approval to commercially release the Flavr Savr tomato, a tomato engineered to have a longer shelf life.^[51] 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.^[52] 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.^[53] 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.^[48] 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.^[54]

GM banana cultivar QCAV-4 was approved by Australia and New Zealand in 2024. The banana resists the fungus that is fatal to the Cavendish banana, the dominant cultivar.^[55]

Methods

Genetically engineered crops have genes added or removed using genetic engineering techniques,^[56] 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^[57]) 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.^[58] 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.^[59] 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.^[60]

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.^[61][62]

In research tobacco and Arabidopsis thaliana are the most frequently modified plants, due to well-developed transformation methods, easy propagation and well studied genomes.^[63][64] 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.

Types of modifications

Transgenic

Transgenic plants have genes inserted into them that are derived from another species. The inserted genes can come from species within the same kingdom (plant to plant), or between kingdoms (for example, bacteria to plant). In many cases the inserted DNA has to be modified slightly in order to be correctly and efficiently expressed in the host organism. Transgenic plants are used to express proteins, like the cry toxins from B. thuringiensis, herbicide-resistant genes, antibodies,^[65] and antigens for vaccinations.^[66] A study led by the European Food Safety Authority (EFSA) also found viral genes in transgenic plants.^[67]

Transgenic carrots have been used to produce the drug Taliglucerase alfa which is used to treat Gaucher's disease.^[68] In the laboratory, transgenic plants have been modified to increase photosynthesis (currently about 2% at most plants versus the theoretic potential of 9–10%).^[69] This is possible by changing the rubisco enzyme (i.e. changing C₃ plants into C₄ plants^[70]), by placing the rubisco in a carboxysome, by adding CO₂ pumps in the cell wall,^[71] or by changing the leaf form or size.^[72][73][74] Plants have been engineered to exhibit bioluminescence that may become a sustainable alternative to electric lighting.^[75]

Cisgenic

Cisgenic plants are made using genes found within the same species or a sexually-compatible closely related one, where conventional plant breeding can occur.^[76] Some breeders and scientists argue that cisgenic modification is useful for plants that are difficult to crossbreed by conventional means (such as potatoes), and that plants in the cisgenic category should not require the same regulatory scrutiny as transgenics.^[77]

Subgenic

Genetically modified plants can also be developed using gene knockdown or gene knockout to alter the genetic makeup of a plant without incorporating genes from other plants. In 2014, Chinese researcher Gao Caixia filed patents on the creation of a strain of wheat that is resistant to powdery mildew. The strain lacks genes that encode proteins that repress defenses against the mildew. The researchers deleted all three copies of the genes from wheat's hexaploid genome. Gao used the TALENs and CRISPR gene editing tools without adding or changing any other genes. No field trials were immediately planned.^[78][79] The CRISPR technique has also been used by Penn State researcher Yinong Yang to modify white button mushrooms (Agaricus bisporus) to be non-browning,^[80] and by DuPont Pioneer to make a new variety of corn.^[81]

Multiple trait integration

With multiple trait integration, several new traits may be integrated into a new crop.^[82]

Economics

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GM food's economic value to farmers is one of its major benefits, including in developing nations.^[83][84][85] 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.^[86][87] Agriculture economists calculated that "world surplus $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%)."^[88]

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.^[89] 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.^[90]

Forgoing these benefits is costly.^[91][92] 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.^[91] They estimate Nigeria alone loses $33–46m annually.^[91] The potential and alleged harms of GM crops must then be compared to these costs of delay.^[91][92]

Critics challenged the claimed benefits to farmers over the prevalence of biased observers and by the absence of randomized controlled trials.^{[citation needed]} 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".^[93]

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.^[94]

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.^{[citation needed]} 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.^[95] 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.^[95]

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.^[89] 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.^[96] As of 2009, the overall Roundup line of products including the GM seeds represented about 50% of Monsanto's business.^[97]

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.^[98] The patent on the first type of Roundup Ready crop that Monsanto produced (soybeans) expired in 2014^[99] and the first harvest of off-patent soybeans occurs in the spring of 2015.^[100] Monsanto has broadly licensed the patent to other seed companies that include the glyphosate resistance trait in their seed products.^[101] About 150 companies have licensed the technology,^[102] including Syngenta^[103] and DuPont Pioneer.^[104]

Yield

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][105]

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.^[105]

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.^[105]

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.^[106] See for example Roundup Ready § Productivity claims.

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.^[107][108]

Traits

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^[109] and insect-resistant brinjal (eggplant).^[110]

Extended shelf life

The first genetically modified crop approved for sale in the U.S. was the FlavrSavr tomato, which had a longer shelf life.^[51] First sold in 1994, FlavrSavr tomato production ceased in 1997.^[111] It is no longer on the market.

In November 2014, the USDA approved a GM potato that prevents bruising.^[112][113]

In February 2015 Arctic Apples were approved by the USDA,^[114] becoming the first genetically modified apple approved for US sale.^[115] Gene silencing was used to reduce the expression of polyphenol oxidase (PPO), thus preventing enzymatic browning of the fruit after it has been sliced open. The trait was added to Granny Smith and Golden Delicious varieties.^[114][116] The trait includes a bacterial antibiotic resistance gene that provides resistance to the antibiotic kanamycin. The genetic engineering involved cultivation in the presence of kanamycin, which allowed only resistant cultivars to survive. Humans consuming apples do not acquire kanamycin resistance, per arcticapple.com.^[117] The FDA approved the apples in March 2015.^[118]

Improved photosynthesis

Plants use non-photochemical quenching to protect them from excessive amounts of sunlight. Plants can switch on the quenching mechanism almost instantaneously, but it takes much longer for it to switch off again. During the time that it is switched off, the amount of energy that is wasted increases.^[119] A genetic modification in three genes allows to correct this (in a trial with tobacco plants). As a result, yields were 14-20% higher, in terms of the weight of the dry leaves harvested. The plants had larger leaves, were taller and had more vigorous roots.^[119][120]

Another improvement that can be made on the photosynthesis process (with C3 pathway plants) is on photorespiration. By inserting the C4 pathway into C3 plants, productivity may increase by as much as 50% for cereal crops, such as rice.^{[121][122][123][124][125]}

Improved biosequestration capability

The Harnessing Plants Initiative focuses on creating GM plants that have increased root mass, root depth and suberin content.

Improved nutritional value

Edible oils

Some GM soybeans offer improved oil profiles for processing.^[126] Camelina sativa has been modified to produce plants that accumulate high levels of oils similar to fish oils.^[127][128]

Vitamin enrichment

Golden rice, developed by the International Rice Research Institute (IRRI), provides greater amounts of vitamin A targeted at reducing vitamin A deficiency.^[129][130] As of January 2016, golden rice has not yet been grown commercially in any country.^[131]

Toxin reduction

A genetically modified cassava under development offers lower cyanogen glucosides and enhanced protein and other nutrients (called BioCassava).^[132]

In November 2014, the USDA approved a potato that prevents bruising and produces less acrylamide when fried.^[112][113] They do not employ genes from non-potato species. The trait was added to the Russet Burbank, Ranger Russet and Atlantic varieties.^[112]

Stress resistance

Plants have been engineered to tolerate non-biological stressors, such as drought,^{[112][113][133][134]} frost,^[135] and high soil salinity.^[64] In 2011, Monsanto's DroughtGard maize became the first drought-resistant GM crop to receive US marketing approval.^[136]

Drought resistance occurs by modifying the plant's genes responsible for the mechanism known as the crassulacean acid metabolism (CAM), which allows the plants to survive despite low water levels. This holds promise for water-heavy crops such as rice, wheat, soybeans and poplar to accelerate their adaptation to water-limited environments.^[137][138] Several salinity tolerance mechanisms have been identified in salt-tolerant crops. For example, rice, canola and tomato crops have been genetically modified to increase their tolerance to salt stress.^[139][140]

Herbicides

Glyphosate

The most prevalent GM trait is herbicide tolerance,^[141] where glyphosate-tolerance is the most common.^[142] Glyphosate (the active ingredient in Roundup and other herbicide products) kills plants by interfering with the shikimate pathway in plants, which is essential for the synthesis of the aromatic amino acids phenylalanine, tyrosine, and tryptophan. The shikimate pathway is not present in animals, which instead obtain aromatic amino acids from their diet. More specifically, glyphosate inhibits the enzyme 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS).

This trait was developed because the herbicides used on grain and grass crops at the time were highly toxic and not effective against narrow-leaved weeds. Thus, developing crops that could withstand spraying with glyphosate would both reduce environmental and health risks, and give an agricultural edge to the farmer.^[143]

Some micro-organisms have a version of EPSPS that is resistant to glyphosate inhibition. One of these was isolated from an Agrobacterium strain CP4 (CP4 EPSPS) that was resistant to glyphosate.^[144][145] The CP4 EPSPS gene was engineered for plant expression by fusing the 5' end of the gene to a chloroplast transit peptide derived from the petunia EPSPS. This transit peptide was used because it had shown previously an ability to deliver bacterial EPSPS to the chloroplasts of other plants. This CP4 EPSPS gene was cloned and transfected into soybeans.

The plasmid used to move the gene into soybeans was PV-GMGTO4. It contained three bacterial genes, two CP4 EPSPS genes, and a gene encoding beta-glucuronidase (GUS) from Escherichia coli as a marker. The DNA was injected into the soybeans using the particle acceleration method. Soybean cultivar A54O3 was used for the transformation.

Bromoxynil

Tobacco plants have been engineered to be resistant to the herbicide bromoxynil.^[146]

Glufosinate

Crops have been commercialized that are resistant to the herbicide glufosinate, as well.^[147] Crops engineered for resistance to multiple herbicides to allow farmers to use a mixed group of two, three, or four different chemicals are under development to combat growing herbicide resistance.^[148][149]

2,4-Dedit

In October 2014 the US EPA registered Dow's Enlist Duo maize, which is genetically modified to be resistant to both glyphosate and 2,4-D, in six states.^{[150][151][152]} Inserting a bacterial aryloxyalkanoate dioxygenase gene, aad1 makes the corn resistant to 2,4-D.^[150][153] The USDA had approved maize and soybeans with the mutation in September 2014.^[154]

Dicambaedit

Monsanto has requested approval for a stacked strain that is tolerant of both glyphosate and dicamba. The request includes plans for avoiding herbicide drift to other crops.^[155] Significant damage to other non-resistant crops occurred from dicamba formulations intended to reduce volatilization drifting when sprayed on resistant soybeans in 2017.^[156] The newer dicamba formulation labels specify to not spray when average wind speeds are above 10–15 miles per hour (16–24 km/h) to avoid particle drift, average wind speeds below 3 miles per hour (4.8 km/h) to avoid temperature inversions, and rain or high temperatures are in the next day forecast. However, these conditions typically only occur during June and July for a few hours at a time.^[157][158]

Pest resistanceedit

Insectsedit

Tobacco, corn, rice and some other crops have been engineered to express genes encoding for insecticidal proteins from Bacillus thuringiensis (Bt).^[159][160] The introduction of Bt crops during the period between 1996 and 2005 has been estimated to have reduced the total volume of insecticide active ingredient use in the United States by over 100 thousand tons. This represents a 19.4% reduction in insecticide use.^[161]

In the late 1990s, a genetically modified potato that was resistant to the Colorado potato beetle was withdrawn because major buyers rejected it, fearing consumer opposition.^[112]

Virusesedit

Plant viruses are a cause of around half of the plant diseases emerging worldwide, and an estimated 10–15% of losses in crop yields.^[162] Papaya, potatoes, and squash have been engineered to resist viral pathogens such as cucumber mosaic virus which, despite its name, infects a wide variety of plants.^[163][162] Virus resistant papaya were developed in response to a papaya ringspot virus (PRV) outbreak in Hawaii in the late 1990s. They incorporate PRV DNA.^[164][165] By 2010, 80% of Hawaiian papaya plants were genetically modified.^[166][167]

Potatoes were engineered for resistance to potato leaf roll virus and Potato virus Y in 1998. Poor sales led to their market withdrawal after three years.^[168]

Yellow squash that were resistant to at first two, then three viruses were developed, beginning in the 1990s. The viruses are watermelon, cucumber and zucchini/courgette yellow mosaic. Squash was the second GM crop to be approved by US regulators. The trait was later added to zucchini.^[169]

Many strains of corn have been developed in recent years to combat the spread of Maize dwarf mosaic virus, a costly virus that causes stunted growth which is carried in Johnson grass and spread by aphid insect vectors. These strands are commercially available although the resistance is not standard among GM corn variants.^[170]

By-productsedit

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