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Biotechnologically Engineered Plants: Comparison
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Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Zareen Khan.

The development of recombinant DNA technology during the past thirty years has enabled scientists to isolate, characterize, and manipulate a myriad of different animal, bacterial, and plant genes. This has, in turn, led to the commercialization of hundreds of useful products that have significantly improved human health and well-being. Commercially, these products have been mostly produced in bacterial, fungal, or animal cells grown in culture. More recently, sScientists have begun to develop a wide range of transgenic plants that produce numerous useful compounds. The perceived advantage of producing foreign compounds in plants is that compared to other methods of producing these compounds, plants seemingly provide a much less expensive means of production. A few plant-produced compounds are already commercially available; however, many more are in the production pipeline.

  • transgenic plants
  • commercialized plants
  • recombinant proteins
  • plants producing pharmaceuticals

1. Early Engineered Plants

Plants that are resistant to insect predation, damage from plant viruses, and various herbicides (used to prevent the growth of weeds) were genetically engineered beginning ~30–40 years ago, and a number of these engineered plants have been commercially available for many years.

1.1. Insect Resistance

Beginning with the 1940s through the 1970s, several powerful chemical insecticides were developed and employed globally on a massive scale. The use of these insecticides had a dramatic effect in reducing the damage to crop plants that resulted from insect predation. The most effective and most widely use of these chemical insecticides was the compound dichlorodiphenyltrichloroethane or DDT [1]. Unfortunately, it was eventually discovered that most of these chemical insecticides, and DDT in particular, had negative effects on animals, ecosystems, and humans [2]. Moreover, many of these chemicals, notwithstanding their apparent effectiveness as insecticides, persisted for many years in the environment and accumulated in increasing concentrations through food chains. With the widespread development of transgenic plants in the early 1980s, scientists began developing plants that were resistant to insect predation [3,4,5,6,7,8,9,10][3][4][5][6][7][8][9][10]. For the most part, this involved isolating genes encoding bacterial insect-toxigenic proteins from various strains of the bacterium Bacillus thuringiensis and expressing those genes in transgenic plants; this approach has turned out to be highly effective and without significant negative consequences. In the past 25 years, the availability and commercial use of transgenic plants expressing one or more of several different B. thuringiensis insecticidal toxins has increased dramatically throughout the US and many other countries of the world [11]. At the present time, 44 countries worldwide (with the notable exception of countries belonging to the European Union) have given regulatory approval to 40 different genetically engineered crops with insect and herbicide-resistant plants being the most commonly introduced traits [12]. Currently, regulatory approved B. thuringiensis-engineered plants include cotton, cowpea, eggplant, maize, poplar, potato, rice, soybean, sugarcane, and tomato.

1.2. Virus Resistance

It has been estimated that there are nearly 2000 known different plant viruses [13], the great majority of which have a small single-stranded RNA genome (often less than 10 kilobases). These viruses can cause significant damage to crop plants, thereby dramatically reducing plant yields. The viral coat protein is generally the most abundant protein in small single-stranded RNA viruses. Consequently, many transgenic plants have been engineered to express a small single-stranded RNA viral coat protein gene and, as a result are often protected against the systematic spread and the subsequent deleterious effects of that virus [14,15,16,17,18,19,20][14][15][16][17][18][19][20]. It is believed that the cloned and expressed viral coat protein gene inhibits the expression of the small single-stranded RNA virus through the mechanism of RNA interference (RNAi). In addition, given the similarity in structure and mechanisms of infectivity of many small plant viruses, the abovementioned viral coat protein gene approach has been found to be highly effective for many different plants, including alfalfa, corn, tobacco, tomato, sugar beet, cucumber, papaya, potato, rice, zucchini, soybean, grapevine, squash, pumpkin, plum, and muskmelon, against several different viruses. Moreover, numerous transgenic plants expressing a small single-stranded RNA viral coat protein gene have been approved by regulatory authorities and subsequently commercialized. Unfortunately, the viral coat protein strategy is only effective when transgenic plants are challenged by closely related viruses. Therefore, scientists have sought to develop transgenic plants that are resistant to a broad spectrum of plant viruses. While several different approaches have been attempted to achieve this end, this remains a work in progress.

1.3. Herbicide Resistance

Every year a large portion of worldwide crop production is lost through weed infestation. This loss of productivity notwithstanding, an estimated ~USD 35–40 billion is spent annually by farmers on >100 different chemical herbicides [21]. Since most herbicides do not discriminate between weeds and crop plants, scientists have developed several different herbicide-resistant crop plants, including plants resistant to triazines, sulfonylureas, imidazolinones, aryloxphenoxypropionates, cyclohexanediones, bromoxynil, phenoxycarboxylic acids, glufosinate, cyanamide, and dalapon. This approach has been so successful that currently ~60% of the transgenic crops that are planted globally have been modified to be herbicide-resistant. However, herbicide-resistant crops do not have a higher yield than non-herbicide-resistant crops [22]. On the other hand, herbicide-resistant crops are preferred for “improved and simplified weed control, less labour and fuel cost, no-till planting/planting flexibility, yield increase, extended time window for spraying, and in some cases decreased pesticide input” [23].
Worldwide, the most widely used chemical herbicide is glyphosate (commercially sold as Roundup®(Bayer, USA), which is claimed by its producer (the Monsanto Corporation, now a division of Bayer) to be safe, cheap, effective, and environmentally friendly [24]. Transgenic plants that have been shown to be resistant to this herbicide include soybean, corn, canola, tobacco, soybean, petunia, tomato, potato, alfalfa, sorghum, sugar beet, Indian mustard, and cotton. Treatment of plants in the field with glyphosate should kill all (or most) of the weeds while the engineered crop plants are not affected. With the widespread acceptance of this herbicide there is, however, some concern that (i) there is too much dependence upon the use of a single herbicide and, as a result, there are numerous instances of weeds acquiring naturally occurring resistance [25,26][25][26]; and (ii) some reports have suggested that long term exposure to this herbicide may be toxic or carcinogenic to humans [27]. Thus, there are some recent literature reports of plants that have been engineered to be resistant to other herbicides that researchers hope will provide an effective alternative to the widespread use of glyphosate [28,29,30][28][29][30]. However, glyphosate is likely to continue to be the dominant herbicide worldwide until some of these newer approaches can be shown to safe and efficacious in the field with a large number of different transgenic plants [31].

2. Pharmaceutical Production

Given the fact that many human therapeutic agents are commercially produced in animal cells in culture, the resultant proteins end up being relatively expensive. This is because animal cells in culture grow slowly, do not produce a large biomass, and require specialized fermentation media and equipment. As an alternative to animal cells, scientists have begun to produce a number of therapeutic proteins in genetically engineered plants (in a process that is euphemistically called pharming). A few of these plant-synthesized pharmaceuticals have been approved for human use while several others are currently being tested in clinical trials (Table 21). For example, one group of scientists showed that transgenic rice could simultaneously produce three functional proteins which together could neutralize HIV-1 [57][32]. These proteins included the monoclonal antibody 2G12, and the lectins griffithsin and cyanovirin-N. This protein mixture enhanced both the activity and the binding of the antibody to the HIV protein gp120, resulting in the virus’s neutralization. Thus, this procedure not only decreased the cost of producing this anti-HIV cocktail, but it also increased the potency of the individual components.
Table 21.
Some plant-synthesized pharmaceuticals.
Product Disease Plant Clinical Trial Status Reference
MB66 HIV-1 and HSV-2 Tobacco Phase I completed [58][33]
Zmapp™ (three chimeric monoclonal antibodies) Ebola virus Tobacco Approved by US FDA in October 2020 [51][34]
VEN BETA Gastroenteritis Rice Preclinical [59][35]
VEN120 Inflammatory bowel disease Rice Phase II [59][35]
Optibumin Loss of albumin Rice Commercialized [60][36]
Vibrio cholerae Cholera Potato Phase I [61][37]
H5N1 influenza virus-like

particle		 Influenza N. benthamiana

(tobacco)		 Phase II [62][38]
H1N1 influenza virus particle Influenza N. benthamiana

(tobacco)		 Phase II [62][38]
Cholera toxin B subunit fused to domain II of dengue virus 2 Cholera and dengue virus Potato Preclinical [63][39]
Taliglucerase alfa Gaucher disease Carrot Approved by US FDA in 2016, commercialized [64][40]
E. coli Heat-labile toxin B Diarrhea caused by enterotoxic E. coli Potato Phase I [65][41]
Aprotinin Reduces surgical bleeding Corn Preclinical [66][42]
Insulin Diabetes Safflower Preclinical [67][43]
Norwalk virus capsid protein Diarrhea Potato, tomato Phase I completed [68][44]
ISOkine™ Growth factor Barley Commercialized [69][45]
Griffithsin, cyanovirin-N HIV, ebola, SARS-CoV-2 Rice Preclinical [57][32]
Abbreviations: HIV-1, human immunodeficiency virus 1; HSV-2, herpes simplex virus 2.
Within the next 15–20 years, many more pharmaceutical proteins are likely to be produced in transgenic plants. Tobacco plants are presently the most popular host for the synthesis of pharmaceutical proteins because of (i) the ease of genetically transforming these plants, (ii) tobacco’s rapid growth, and (ii) the large size of the tobacco leaf, which yields large amounts of the target protein [70][46]. However, in an effort to determine the optimum plant host for foreign proteins, scientists are currently expressing pharmaceutical proteins in a range of different plants. Other plants that have been used to produce foreign proteins include maize, wheat, tomato, potato, mustard, banana, rice, and soybean. For example, some pharmaceutical proteins have been synthesized in rice kernels, which are subsequently ground into a powder and put into easy-to-deliver and consume gelatin capsules. It is important to keep in mind that the purification of plant-produced proteins may present unique challenges and is certainly expected to be different from purifying the same protein from animal cells in culture. Using traditional techniques (i.e., Agrobacterium tumefaciens’ transformation of plants) to produce pharmaceutical proteins may be effective; however, it is a relatively time-consuming and labor-intensive process [71][47]. On the other hand, this approach is currently being replaced by transient expression systems as well as the use of plant cell cultures [71][47] wherein the time to produce a foreign protein may be reduced by 10-fold or more. Unfortunately, these approaches are currently significantly more expensive than relying on A. tumefaciens’ transformation followed by plant growth. As a consequence of concerns among both the public and the scientific community that transgenic plants producing pharmaceuticals could threaten traditional agriculture, the environment and/or human health, it is currently necessary to grow these plants under contained conditions [72][48]. However, using transient expression systems as well as plant cell cultures should enable scientists to safely produce large amounts of pharmaceuticals in plants.

3. Fungal and Bacterial Resistance

Plant pathogens reduce crop yields by adversely affecting plant growth and development. It has been estimated that diseases globally reduce crop yields by 20–40% [163][49]. In the past decade, there has been a surge in the use of genome editing technologies in generating crops that are resistant to a wide range of pathogens. Several studies of targeted mutagenesis in crop plants, including deletions, insertions, and replacement of DNA of various sizes at targeted sites, have proven to be a promising approach to improve plant resistance to pathogens. Developing plant resistance by modifying host S genes such as those belonging to the mlo (Mildew Resistant Locus O) gene family has been effective in apple, tomato, barley, and wheat [164][50]. However, a common disadvantage of S gene mutation is the concomitant negative impact on plant growth and productivity [165,166][51][52]. Therefore, a CRISPR/Cas9-induced targeted deletion in the MLO-B1 locus resulted in a mutant wheat variety (Tamlo-R32) that thrived better and maintained growth and yields while conserving resistance to powdery mildew [167][53]. In another study conducted by Peng et al. [168][54] on citrus plants, CRISPR/Cas9-targeted modification of the S gene CsLOB1 was performed to enhance resistance to citrus canker. Some recent experiments on rice reported the use of CRISPR/Cas9 technology to induce mutagenesis in the promoter region of bacterial blight S genes, OsSWEET14 and OsSWEET11 [169][55]. Antony et al. [170][56] developed blight-resistant rice plants with an OsSWEET14 TDNA insertion mutant but when compared to wild-type plants the mutants had smaller seeds. In contrast, resistance against rice blight with no growth defects was detected in the TALE-edited OsSWEET14 gene in super basmati rice [171][57]. These results suggest that engineering S genes through genome editing technology is a potential strategy to enhance rice resistance to blight caused by Xanthomonas oryzae pv. Oryzae. Thus, with rice production threatened by bacterial blight causing major crop losses, rapid and durable methods are desperately needed. In addition to the knockout of host genes to improve disease resistance, endophyte-derived genes can serve as additional routes for improvement of wheat traits. In a recent study by Wang et al. [172][58], the authors identified a Fusarium resistance gene (Fhb7), which was shown to be horizontally transferred from an endophytic fungus and conferred resistance to Fusarium head blight (FHB), a significant fungal disease of wheat. The researchers demonstrated that introgression of Fhb7 into the genome of many commercial wheat cultivars conferred tolerance to FHB without negatively affecting growth yields, suggesting that Fhb7 is a potential candidate for engineering blight resistance in elite wheat varieties. Similarly, in tomato plants, CRISPR/Cas 9-mediated knockout of the DMR6 gene enhanced resistance to bacterial pathogens including P. syringae, P. capsici, and Xanthomonas spp., with no adverse effects on plant development and growth. As more targets are identified, it is expected that there will be many more successful studies on durable and broad-spectrum disease resistance using the CRISPR/Cas9 approach in a wide range of crops. The effect of overexpression of plant proteins such as ribosome-inactivating proteins (RIPs) on performance of fungal and bacterial pathogens has been investigated [173][59]. Some interesting examples, such as overexpression of the PhRIP gene in transgenic potato, protected the plants against damage from Botrytis cinerea and Rhizoctonia solani, whereas expressing the RIP alpha-MMC gene improved resistance to rice blast fungus in rice [174,175][60][61]. Other proteins, including PFLP (plant ferredoxin-like protein) and HRAP (hypersensitive response-assisting proteins), are effective against multiple bacterial pathogens when they are overexpressed in rice, banana, and other species [176,177][62][63]. Recently, overexpression of PFLP and HRAP genes in greenhouse and field-grown bananas indicated that both genes are effective against bacterial wilt caused by Xanthomonas spp. [178][64]. In an earlier study, a combination of both genes did not provide any additional benefits in banana, yet the authors speculate that bananas expressing both genes may be more durable [179][65]. Furthermore, the disease-resistance trait was passed on to the next generation of transgenic lines. Additionally, the authors noted no difference in the agronomic traits, including yield and flowering of field-grown symptom-free bananas. These examples are helpful in revealing the biological function of plant proteins that can be beneficial when engineering crop tolerance to pathogen attacks. Harpins may act in extracellular spaces in plant tissue, facilitating recognition by the plant [180][66]. Harpins are effective against multiple pathogens when overexpressed in tobacco, rice, canola, and cotton [181,182,183,184,185][67][68][69][70][71]. The effect of overexpression of harpinxooc encoding the hrf2 gene on the performance of an oomycete pathogen was investigated by Niu et al. [186][72]. The results demonstrate that transgenic soybeans expressing the hrf2 gene showed enhanced resistance to Phytophthora sojae. This study provides a valuable insight toward the functional role of the hrf2 gene in plant defense against P. sojae, opening new avenues for understanding other important pathogens as well as subsequently engineering broad-spectrum disease resistance in soybean. The ability of plants to utilize diverse classes of immune receptors to perceive the presence of pathogenic microbes makes possible the transferring and engineering of these receptors to improve recognition capacities [187][73]. Recently, Ercoli et al. [188][74] conducted studies to show how the XA21 receptor in rice recognizes and resists infection caused by Xanthomonas oryzae. Other immune receptors have been targeted for modification in potato, apple, and rice. A late blight-resistant potato with a NOD-like receptor (NLR) introduced from a wild relative is currently on the market in the UK [12]. In apples, modification of the HcrVf2 gene encoding such a receptor conferred resistance against the devastating fungal scab Venturia inaequalis [189][75]. Xu and colleagues [190][76] showed that rice plants constantly expressing an immune regulator gene, NPR1 (non-expressor of pathogenesis-related genes 1), conferred resistance to bacterial blight but displayed growth defects. However, when the authors controlled NPR1 expression, it resulted in increased accumulation of NPR1 upon pathogen infection, enhancing resistance to bacterial blight without negatively affecting plant growth and grain yield. Although this method enables researchers to obtain plants with strong immunity, durability can be challenging because pathogens are evolving rapidly. An important strategy in the fight against Verticillium wilt (VW), caused by fungi belonging to the genus Verticillium, is to silence genes essential for spore production, hyphal development, and pathogenicity. RNAi-mediated silencing of the VdRGS1 gene has been achieved in cotton, resulting in transgenic plants with enhanced resistances to VW. With the help of RNAi technology, Govindrajulu et al. [191][77] showed that the transgenic lettuce containing a modified construct of highly abundant message #34 (HAM34) and cellulose synthase (CES1) genes showed resistance against a biotrophic pathogen that causes downy mildew of lettuce. Similarly, a PsFUZ7 RNAi construct expressed in transgenic wheat conferred strong resistance to wheat stripe rust. Additionally, knocking down the transcription factor gene OsERF922 (ethylene responsive factor) using RNAi results in increased resistance against the pathogen Magnoporthe oryzae [192][78]. The improvement of rice blast resistance via CRISPR/Cas9, which targeted knockdown of the OsERF922 gene in a japonica rice variety cultivated in northern China, was reported by Wang et al. [193][79]. This modification led to no detrimental effects on rice growth and development. Overall, RNAi appears to be a promising approach to control the detrimental effects of many fungi and oomycetes.

4. Increasing Plant Yield

One of the main objectives of growing plants, whether the plants are transgenic or non-transgenic, is to increase the yield of the target plant. Moreover, plant yield is important whether the plant is intended to be used as a food or as the source of a cloned protein. In addition, increasing crop yields can decrease the amount of land that is required for agricultural production [194][80]. In recent years, scientists have developed several unique schemes intended to increase the yield of various plants. For example, one group of scientists developed an approach that they called ‘speed breeding’ that is applicable to essentially all crops [195][81]. Speed breeding entails extending the plant’s photoperiod, controlling the plant’s growth temperature, and selection of fast-growing seeds. Of course, to more rapidly grow plants, controlling their growth environment requires the extensive use of greenhouses. In this environment, the lighting may be supplemented with artificial electric lamps [196][82], the photoperiod may be extended [197][83], and the wavelength of the lighting may be altered [198][84]. Following these protocols, researchers have reduced the growth cycle of many different plants to an average of half of what it was previously, thereby enabling the controlled growth of additional generations of the same plant [195][81]. Scientists have developed several different schemes in an effort to increase plant crop yields. For example, traditional varieties of wheat and rice allocate a significant fraction of their resources to producing vegetative tissues rather than grain or reproductive tissues [199][85]. However, semi-dwarf varieties previously developed by conventional breeding during the so-called green revolution [200][86] allocate a greater portion of their resources to grain rather than to vegetative (leaf) tissues. By genetic modulation of the levels of the phytohormones gibberellin and brassinosteroid, it should be possible to produce dwarf plant strains that allocate even more resources to grain instead of vegetative tissues, and thereby further increase the grain yield. In another study, researchers observed that they were able to genetically modify tomato plants to increase their harvest index, which is the ratio of fruit yield to total plant biomass [201][87]. This was accomplished by introducing a chloroplast-targeted cyanobacterial flavodoxin gene into tomato plants. In this case, the transgenic plants were generally smaller than the wild-type plants with a higher number of tomato fruits per plant. Moreover, the overall yield of tomato fruit could be augmented by increasing the density of plants in the field (i.e., by planting the transgenic plants close together). In a separate study, scientists increased the expression of the maize (corn) MADS-box transcription factor gene zmm28 by placing this gene under the control of a moderate-level constitutive maize promoter [202][88]. In field trials, the transgenic plants with increased expression of the zmm28 gene showed an increase in carbon assimilation, nitrogen utilization, and plant growth, all leading to an increase in grain yield relative to the cultivar of wild-type maize used in this study. Methylation of the N6 position of adenosine residues in RNA molecules is common in plants (as well as in other higher eukaryotes), and this modification is believed to regulate RNA processing and metabolism [203][89]. In a recent experiment, scientists introduced and expressed the human demethylase FTO gene into rice and potato plants [204][90]. Expression of this transgene resulted in an exceptionally large increase in rice grain yields in plants that were grown in the greenhouse and a smaller, although still highly significant, increase in rice and potato yield and biomass when plants were grown in the field. In this experiment, expression of the transgene caused an increase of root meristem proliferation and tiller bud formation as well as overall plant photosynthetic efficiency and drought tolerance, suggesting that modulating RNA methylation is an effective way to improve plant yield. Scientists who generated transgenic rice by overexpressing the rice gene encoding a plasma membrane H+-ATPase 1 gene (i.e., OSA1) found that the resultant transgenic plants significantly improved their utilization of nitrogen and carbon resources compared to wild-type [205][91]. As a result of this manipulation, the transgenic plants showed a large increase in grain yield. In addition to introducing exogenous genes to increase plant yield, some researchers have used the CRISPR/Cas9 system to modify some of the existing plant genes (i.e., this technique enables scientists to directly alter specific plant genes) to achieve the same ends as genetic transformation [206][92]. In one instance, in the T2 generation following the genomic modification, three of the four rice plant mutants that were created yielded an increased number of rice grains and had a larger grain size. Also using the CRISPR/Cas9 system, the alteration of multiple genes in a single tomato cultivar worked together to affect the yield of rice. In this case, the CRISPR/Cas9 system was used to edit six independent loci that were important for controlling the yield and productivity in a wild tomato (Solanum pimpinellifolium) crop line [150][93]. When the engineered tomato plant was compared to the wild-type plant, it was observed to have a three-fold increase in fruit size and a ten-fold increase in fruit number. In addition to these examples, researchers have used the CRISPR/Cas9 system to modify an already shortened version of canola (by conventional breeding) so that the plant has more branches, resulting in the formation of more flowers and pods. This was achieved by knocking out genes for receptors that perceive the hormone strigolactone [207][94]. Another group of researchers used the CRISPR/Cas9 system to knock out the rice OsPDCD5 gene, which is involved in programmed cell death [208][95]. Mutating this gene decreased auxin synthesis by the modified plant in addition to lowering gibberellin and cytokinin synthesis and signaling pathways. Moreover, rice that contained mutations in the OsPDCD5 gene had an increased yield of rice grains. From the above cursory exploration of some strategies that have been employed to increase plant fruit or grain yield, it is clear that plant yield is controlled by a relatively large number of different genes. The expression of some of these genes may be increased while the expression of others is decreased with the same ultimate result, i.e., the yield is increased. Moreover, in some instances, the addition of foreign genes may also result in an increase in yield. While most of these genetic manipulations have yet to be tested and proven in the field, there is every reason to expect that the approaches described here will eventually lead to plants with much greater fruit, seed, and grain yield than is currently available from wild-type plants, including plants that have been manipulated by traditional breeding techniques.

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