An Update On Genetically Modified Crops

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An update on genetically modiﬁed crops
Article in Ciencia e Investigación Agraria · December 2008

DOI: 10.4067/S0718-16202008000300001
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Cien. Inv. Agr. 35(3): 231-250. 2008
www.rcia.puc.cl
revision de literatura
An update on genetically modified crops
Andrés R. Schwember
Department of Plant Sciences, University of California, Davis, CA 95616-8780, USA
Abstract
A. R. Schwember. 2008. An update on genetically modified crops. Cien. Inv. Agr. 35(3):231-
250. Genetically modified (GM) crops were introduced in the mid 1990s and two principal
transgenic technologies currently dominate the market, herbicide-tolerant (HT) crops and insect-
resistant crops (Bacillus thuringiensis (Bt) crops). HT crops have simplified weed management
practices, reduced crop production costs, and have had positive effects on the environment.
However, there are concerns about the potential development of weeds resistant to glyphosate,
the main herbicide employed with HT crops. A second major worry associated with the use of
HT crops is the potential introgression of genes from GM crops into wild relatives (i.e. gene
flow) and its potential impact on natural ecosystems. Bt crops have increased yields and reduced
the use of insecticides, providing benefits for human health and the environment. However, the
potential development of resistance to the Bt toxin by insect pests and the indirect damage of
Bt toxins to non-target species are major concerns related to their use. Different strategies to
mitigate and eliminate the problems associated with the use of GM crops are discussed in the
paper. The next step in plant biotechnology is the release of nutritionally-enhanced components
in seeds that will benefit humans directly.
Key words: Bt crops, gene flow, genetically modified crops, glyphosate, Golden Rice,
herbicide-tolerant crops, transgenic crops.
Introduction An important breakthrough in the development

of GM crops occurred when Murai et al. (1983)
Genetically modified (GM), genetically produced sunflower tissues carrying a seed protein
engineered, or transgenic crops refer to gene from French bean, and these authors were
plants produced by the insertion of specific the first to demonstrate the expression of a plant
pieces of nucleic acids into the plant’s DNA gene after transfer to a taxonomically distinct
using recombinant DNA technology (i.e. botanical family. However, more than a decade
Agrobacterium-mediated transformation or passed before the release of the first commercial
direct gene transfer methods) (Griffiths et al., GM crops. In 1994, ‘FlavrSavr’ fresh tomatoes
2005). This biotechnological approach allows from Calgene (now Monsanto) and processing
genes to be introduced into a plant genome tomatoes developed in the United Kingdom
from any source (i.e., plant, animal, bacterial, (UK) were developed and commercialized.
fungal) resulting in the potential transfer of Transgenic techniques were used in these first
a wide range of genetic resources between GM tomato varieties to reduce the activity of
unrelated species, a major difference compared a gene encoding polygalacturonase, an enzyme
to traditional plant breeding that is limited to that contributes to cell wall softening during
exchange of genetic material only between ripening, which slowed down the ripening
sexually compatible close relatives of a given process and extended the shelf life of GM
plant (Mirkov, 2003). tomato varieties (Smith et al., 1988). ‘FlavrSavr’
was shortly withdrawn from the market since the
trait was not originally introduced into a suitable
Received 17 December 2007. Accepted 17 March 2008. genetic background and the tomato did not
1
Corresponding author: [email protected] perform well in commercial production (Slater et
232 CIENCIA E INVESTIGACION AGRARIA
al., 2003). The GM processing tomatoes turned agriculture (Halford, 2006). Global adoption
out to be much more successful because of the rates for GM crops have grown over 10% each
higher solids content compared to conventional year since 1996 and are projected to continue to
varieties, reducing the cost of processing, but grow at this rate (Figure 1). Countries with the
most retailers withdrew it in 1999 in response greatest number of biotech crop hectares are (in
to anti-GM attitudes from consumers (Halford, million of hectares) the USA (57.7), Argentina
2006). (19.1), Brazil (15.0), Canada (7.0), India (6.2),
and China (3.8). GM soybean continued to be
The main introduction of GM crops took place the principal biotech crop in 2007, occupying
in 1996, when biotechnology-derived herbicide- 58.6 million hectares (51% of global GM crop
tolerant (HT) and insect-resistant traits were area), followed by corn (31%), cotton (13%)
launched into the market in soybean, cotton, and canola (5%) (James, 2007). There are
corn, and canola (Table 1). These ‘input traits’ also commercial sugar beet, squash, papaya,
were designed to benefit the farmer directly tobacco, and carnation GM crops available in
and aimed to increase productivity per hectare, the markets of the USA and other countries,
reduce agrochemical use, decrease production although with much smaller areas of cultivation.
costs, have greater flexibility and efficiencies in Since 1996, HT has consistently been the
production regimes, and improve grower health dominant trait followed by insect resistance
(Hossain et al., 2004; Huang et al., 2005). and stacked (combined) genes for these two
However, the recent emergence of herbicide traits. In 2007, HT, deployed in soybean, corn,
resistant weeds due to the repetitive use of canola, and cotton occupied 63% (72.2 million
herbicides with the same mode of action in hectares) of the global biotech market, with
fields of HT crops has posed serious concerns 20.3 million hectares (18%) planted to Bt crops
about the sustainability of the weed control and 21.8 million hectares (19%) to the stacked
provided by HT crops. Another constraint is traits of Bt and herbicide tolerance. The stacked
the potential appearance of weedy relatives trait products were the fastest growing trait
resistant to those herbicides by cross pollination group between 2006 and 2007 at 66% growth,
to HT crops (Sanvido et al., 2007). There are compared with 7% for insect resistance and 3%
additional worries about the sustainability and for herbicide tolerance (James, 2007).
durability of pest resistance as a result of the
increasing and uninterrupted use for more than The USA has been the world leader in the
one decade of modified Bacillus thuringiensis field of agricultural biotechnology, and the
toxins (Bt), which confer insect-resistance to adoption of GM crops has steadily grown in
GM crops (Bt crops) (Christou et al., 2006). the country (Figure 2). Based on USDA survey
data, from 1997 to 2007 HT soybean increased
The objectives of this review are to analyze from 17% to 91% of the total US soybean area.
the current worldwide scenario of the main Plantings of HT cotton expanded from 10%
commercialized GM crops since their in 1997 to 70% in 2007 of the total US cotton
introduction in the mid nineties, give an area, whereas HT corn reached 52% of US
overview about why and how these GM crops corn area in 2007 (Fernández-Cornejo, 2007).
were developed, examine the advantages and Regarding the insect-resistant crops, plantings
risks of using these transgenic crops, and explore of Bt corn grew from 8% of the total US corn
the new trends encompassing GM crops. area in 1997 to 49% in 2007 while plantings of
Bt cotton expanded from 15% in 1997 to 59%
Current status of GM crops in 2007. The adoption of stacked varieties of
cotton and corn reached 42% and 28% of US
In 2007, 12 million growers planted around plantings in 2007, respectively (Fernández-
114 million hectares worldwide of crops Cornejo, 2007). Second-generation products
having biotechnology-derived traits across 23 entered the American market in 2003 with the
countries, with an overall estimated market introduction of Bollgard® II cotton (Table 1).
value of U$ 6.9 billion (James, 2007) and Features of second-generation products include
representing approximately 6% of worldwide the stacked genes, two modes of action (i.e., two
VOL 35 N˚3 SEPTIEMBRE - DICIEMBRE 2008 233
Table 1. Examples of commercially available genetically modified crops.
Crop Trait Target Trait Originating Year of first Trade

phenotype trait gene(s) designation company commercial sale name

Cotton Resistance1 to cry1Ac MON531 Mosanto 1996 Bollgard®,
lepidopteran Ingard®
cry1Ac, MON15985 Monsanto 2003 Bollgard® II
cry2Ab2
cry1Fa, 281-24-236 x Dow AgroSciences 2005 WideStrikeTM
cry1Ac, pat 3006-210-23
Resistance to CP4 epsps MOB1445/1698 Monsanto 1996 Roundup
glyphosate Ready®
herbicides
Resistance to bar LLCotton25 Bayer CropScience 2005 LibertyLink®
phosphinothricin
herbicides
Corn Resistance1 to cry1Ab, pat Bt11 Northrup King 1996 YieldGard®
European corn (now Syngenta) Attribute®
borer and other
lepidopteran insects
cry1Ab MON810 Monsanto 1997 YieldGard®
Corn Borer
cry1F, pat TC1507 Dow AgroSciences; 2003 Herculex® I
Pioneer Hi-Bred Intl
Resistance1 to cry3Bb1 MON863 Monsanto 2003 YieldGard®
corn rootworm Rootworm
cry1Ab, MON863 x Monsanto 2005 YieldGard® Plus
cry3Bb1 MON810
Resistance to Maize epsps GA21 DeKalb (now Monsanto) 1998 Roundup Ready®
glyphosate
Two CP4 NK603 Monsanto 2001 Roundup Ready®
epsps Corn 2
expression
cassettes
Resistance to pat T14, T25 Aventis 1996 LibertyLink®
phosphinothricin (now Bayer CropScience)
herbicides
Soybean Resistance to CP 4 epsps GTS-40-3-2 Monsanto 1996 Roundup Ready®
glyphosate
herbicides
Canola Resistance to CP 4 epsps, GT73 Monsanto 1996 Roundup
glyphosate gox v247 Ready®
herbicides
Resistance to pat Topas 19/2 AgrEvo 1995 LibertyLink®
phosphinothricin (now Bayer CropScience)
herbicides
Alfalfa Resistance to CP 4 epsps J101, J163 Monsanto 2005 Roundup Ready®
glyphosate
herbicides
Squash Resistance1 to Coat protein CZW3 Asgrow; Semini 1998 Destiny III,
CMV, WMV2 genes of, Vegetable Seeds (now Monsanto) Conquerer III,
and ZYMV CMV, WMV2 Liberator III
and ZYMV
Resistance1 to Coat protein ZW-20 Asgrow; Semini 1995 Preclude II,
WMV2 and genes of Vegetable Seeds Patriot II,
ZYMV WMV2 and (now Monsanto) Declaration II,
ZYMV Independence II
Papaya Resistance1 to PRSV coat 55-1 Cornell university; 1998 SunUp, Rainbow
protein gen 63-1 University of Hawaii,
PRSV USDA
1
Many insect resistance and herbicide resistance traits are also available in combinations as stack traits. This table contains representative
traits and is not an exhaustive list of all global commercial traits. CMV, Cucumber mosaic virus; PRSV, Papaya ringspot virus; WMV2,
Watermelon mosaic virus; ZYMV, Zucchini yellow mosaic virus (Castle et al., 2006). Reproduced with permission of the publisher.
140
120 Total
Million hectares, 1996-2007

Industrial
100 Developing
80
60
40
20
0
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007
Years
Figure 1. Worldwide grown area of transgenic crops between 1996 and 2007. Increase of 12%, 12.3 million hectares (30
million acres) between 2006 and 2007.
different Bt genes combined in one product) (Gianessi, 2005). The most successful HT traits
for improved insect resistance management, introduced to date have enabled GM crops to
and enhanced performance of the traits (i.e., grow in the presence of foliar-applied, broad-
increased spectrum of the target insects). For spectrum and non-selective herbicides, such as
example, WidestrikeTM cotton and YieldGard® glyphosate and glufosinate. Both compounds
Plus corn are recently released products with are amino acid analogues that have molecular
stacked Bt gene traits (Castle et al., 2006). targets in the amino acid biosynthetic pathways
(Slater et al., 2003).
Commercialized GM crops
Glyphosate is the only herbicide that acts by
Herbicide-tolerant (HT) crops blocking the shikimate pathway though specific
inhibition of the enzyme 5-enolpyruvyl-
HT GM crops were developed to simplify weed shikimate-3-phosphate synthase (EPSPS)
management and reduce the associated costs (Figure 3). The inhibition of EPSPS impairs
Percent of acres
100
HT
Soybeans
180 HT Cotton
Bt Cotton
HT Cotton
Percent of acres
Bt Corn
160
140
120
100
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007
Years
Figure 2. Adoption of transgenic crops grows steadily in the USA. Reproduced with permission of the author.
the biosynthesis of aromatic amino acids required for the assimilation of nitrogen into
and causes misregulation of the shikimate the amino acid glutamine. The bar gene used
pathway (Duke et al., 2003), affecting normal to produce plants resistant to glufosinate was
plant growth. The development of glyphosate- isolated from the bacterium Streptomyces
resistant crops (GRCs) utilized the CP4 gene hygroscopicus and encodes a phosphinothricin
from Agrobacterium sp., which encodes a acetyl transferase (PAT), an enzyme that
glyphosate-resistant form of EPSPS, initially detoxifies the herbicide through acylation
introduced in soybean (Padgette et al., 1996). (Thompson et al., 1987). Many crop species have
The vast majority of the commercial GRCs on been successfully transformed with this gene.
the market today contain the CP4 EPSPS gene However, since 1997, only glufosinate-resistant
that confers glyphosate resistance (Dill, 2005). canola, cotton, and corn have been introduced
Glyphosate-resistant canola also contains a in the USA with moderate success. Glufosinate-
gene that encodes a glyphosate oxireductase resistant canola has been particularly successful
(GOX) from Ochrobactrum anthropi. This in Canada (Halford, 2006).
enzyme degrades glyphosate to glyoxylate,
a safe and ubiquitous natural product, and There are several health and environmental
aminomethylphosphonate (AMPA), a non-toxic benefits associated with the use of glyphosate
compound (Duke, 2005). and glufosinate, as opposed to other chemical
herbicides. Both compounds are considered
Glufosinate (or phosphinothricin) is a competitive more toxicologically benign than many of the
inhibitor of glutamine synthetase, an enzyme herbicides they replace (Ebert et al., 1990;
Williams et al., 2000) due to their relatively
short soil half-lives and low mobility to
ground or surface water (Duke et al., 2003).
Shikimic Acid
In a comprehensive review, Cerdeira and Duke
Shikimate kinase
(2006) concluded that the environmental effects
of glyphosate on contamination of water, air,
Shikimic Acid-3-Phosphate soil and non-target organisms are minimal
relative to some of the herbicides they replace.
In addition, the authors gave extensive evidence
EPSP
Glyphosate X +PEP
Synthase
that no risks have been found with food, feed
5-EnolPyruvyl Shikimic Acid -3-Phosphate safety, or nutritional value in products from
currently available glyphosate-resistant crops
(GRCs). However, the drift of glyphosate to non-
Chorismate Synthase
target plants represents a direct environmental

Chorismic Acid
impact (Ellis et al., 2003), which is a problem
associated with all foliar-applied herbicides.
Chorismic Acid Anthranilic Acid
One of the most significant environmental
benefits of using glyphosate and glufosinate
on HT crops has been the rapid conversion to
Phenilalanine Tyrosine Tryptophan
reduced-, minimum- and no-tillage agriculture
(Cerdeira and Duke, 2006). In conventional
agriculture, mechanical cultivation and
Figure 3. Glyphosate mode of action (Dill, 2005). Three incorporation of soil-applied herbicides
basic biotechnological strategies have been evaluated
have been important components of weed
in order to introduce glyphosate resistance into crops
species: (1) Over-expression of the sensitive target management, resulting in loss of topsoil with
enzyme, (2) Detoxification of the glyphosate molecule, sometimes irreversible environmental damage.
and (3) Expression of an insensitive form of the target In contrast, these practices are less utilized
enzyme. This last strategy has been the most successful
with foliar-applied compounds (i.e., glyphosate
in glyphosate-resistant crops, in which the CP4 gene from
Agrobacterium sp. encodes a glyphosate-resistant form of and glufosinate), which kill almost all weeds
EPSPS (Dill, 2005). without tillage. Recently, the University of
São Paulo in Brazil reported that growing HT areas of transgenic glyphosate-resistant crops
soybeans with conventional tillage produced in Argentina and Brazil, there are now evolved
topsoil losses of 1.2 tons per hectare, whereas glyphosate-resistant populations of Sorghum
the glyphosate-resistant soybean planted with halepense and Euphorbia heterophylla,
no-till practices shrank soil losses to 0.2 tons respectively (Powles, 2008). The scale of the
per hectare, a reduction of more than 80% occurrence of glyphosate-resistant weeds
with respect to conventional tilling practices remains small. Nevertheless, agricultural experts
(Service, 2007). Glyphosate-resistant soybeans worry that an epidemic of glyphosate-resistant
have been very instrumental in the fast weeds might start in the short term and become
conversion to minimum tillage agriculture in a problem (Service, 2007; Powles, 2008).
the USA, and glyphosate-resistant cotton has
contributed to the introduction of minimum- Introgression (gene flow) of herbicide tolerance
tillage cotton (Carpenter and Gianessi, 1999). transgenes from GM crops into wild relatives
Furthermore, it has been estimated that has the potential to exacerbate problems
complete conversion to no-till can save as much with existing weed species in HT crops or to
as 53 liter.ha-1 in fuel alone, depending upon the increase the aggressiveness of those species that
number of trips eliminated from production are not generally considered weeds (Sanvido
practices (Dill, 2005). The use of glyphosate in et al., 2007). This has been considered a
GRCs can eliminate the need for cultivation for legitimate concern of environmentalists and an
weed control, allowing growers to reduce row unalterable effect that GM crops might cause
spacing when planting soybeans from 76 to 33 (Duke, 2005). Studies show that transgenes
cm and less. This effectively provides earlier for herbicide resistance are almost certain to
and faster canopy closure by the crop, which move from herbicide-resistant canola to weedy
further reduces weed competition (Dill, 2005). relatives (Légère, 2005), and transgene flow
from cultivated rice to its wild relatives has
The appearance and spread of HT weeds as also been documented (Chen et al., 2004).
a result of the cultivation of HT crops have Gene flow from glyphosate-resistant creeping
been an important concern for growers, bentgrass (Agrostis stolonifera) has caused
environmentalists and scientists. HT crops can additional concerns (Watrud et al., 2004). In
influence herbicide-resistant weeds in several summary, gene flow has to be considered a
ways: (i) naturally HT weed species can replace legitimate limitation of GM crops and will be
those species effectively controlled by the further discussed below.
herbicide employed with the resistant crop; (ii)
the herbicide utilized with the resistant crop can There has been controversy whether the
exert strong selection pressure on weed species, introduction of HT crops reduced the amount
causing the appearance of resistant biotypes; of applied herbicide. Overall, several studies
and (iii) the HT crop could become a persistent support a small but statistically significant
weed in a different crop system. However, these reduction in herbicide use after the adoption of
issues are not new to growers and pose no more HT crops (Sanvido et al., 2007).
environmental problems than those occurring
since herbicides were introduced in the middle Insect resistance
of the last century (Duke, 2005). To date
between eleven (Heap et al., 2006) and twelve The insecticidal properties of the parasporal
(Service, 2007) species of weeds have evolved crystal (protein) of Bacillus thuringiensis
resistance to glyphosate, although only three (Bt) have been used as an alternative to
of these cases (Conyza canadensis, Ambrosia conventional insecticides for around 60 years
artemisiifolia, and Amaranthus palmeri) have and have been the principal insect resistance
been associated with GRCs, ten years after their GM technology employed to date. Bacillus
introduction (Cerdeira and Duke, 2006). There thuringiensis is a ubiquitous soil bacterium that
are new evolved glyphosate-resistant species of synthesizes proteins with insecticidal properties
Conyza, Ambrosia and Lolium that have been (δ-endotoxins or crystal (Cry) proteins)
recently reported in the USA. Likewise, in characterized by a relatively narrow range of
activity. Bt crystal proteins are ingested by from 22% to less than 5% based on a survey
insects and subsequently dissolved in the insect made in 1999 (Huang et al., 2002). In the Yellow
midgut under alkaline conditions, resulting River cotton-growing region in northern China,
in a protoxin of ~130 kDa. The protoxins are over 4 million small farmers have exhibited
subsequently trimmed by gut proteases to an comparable results in insecticide use reduction
N-terminal, 65-70 kDa truncated form, which (Pray et al., 2002). In pre-commercialization
represents the activated toxin. The toxin binds trials, Bt rice has also shown benefits to small
to specific receptors on the cell membranes of and poor farm households in China with 6-9%
the midgut epithelial cells, inserts itself into the higher crop yields and 80% reduction in pesticide
membrane, and forms membrane pores that kill use (Huang et al., 2005). The yield advantages
the epithelial cells (and eventually the insect) of Bt crops relative to non-transgenic crops are
by osmotic lysis (Knowles and Dow, 1993; de less pronounced in developed countries such
Maagd et al., 1999). Toxicity can be correlated as the USA, where yield increases are less
with the number and type of receptors of the than 10% for Bt cotton and Bt corn, as insect
target insect species. Resistant insects show pests already are largely controlled through
alterations in the receptor that binds to the toxin use of other insecticides (Lauer and Wedberg,
(Van Rie et al., 1990; Tabashnik, 1994). 1999; Carpenter et al., 2002). However, the
environmental and economic gains of pesticide
Bt crystal proteins are part of a large and savings and reduced effort for insect control
growing protein family (around 410 toxins, are well documented in the literature, such as
Crickmore et al. (2007)) and their high the case of Bt cotton grown and evaluated in 81
selectivity is to a large extent determined by the commercial fields in Arizona (USA) (Cattaneo
toxin-receptor interaction (Van Rie et al., 1990). et al., 2006). In this study, transgenic and non-
The members of the Cry gene family were transgenic cotton had similar yields overall,
originally grouped in subfamilies according largely because higher insecticide use with
to their selectivity for members of the insect non-transgenic cotton improved control of key
families Lepidoptera (moths and caterpillars), pests. Another study conducted by FAO (2004)
Diptera (flies and mosquitoes), and Coleoptera revealed that the average number of insecticide
(beetles) (Höfte and Whiteley, 1989), which are applications in the USA used against the
the primary targets of the Bt toxins (MacIntosh budworm-bollworm complex decreased from
et al., 1990). The current nomenclature is based 4.6 in 1992-1995 to 0.8 in 1999-2001, largely
solely on amino acid identity and removes the owing to the introduction of Bt cotton.
necessity for researchers to bioassay each new
toxin against a growing series of organisms The potential development of resistance to
(Crickmore et al., 2007). Due to the high the Bt toxin is the major concern related to
specificity of the toxin, Bt crops have resulted the use of Bt crops. The diamondback moth
in no significant risk to human health and the (Plutella xylostella) is the only pest to have
environment compared with the chemical evolved resistance to Bt sprays used by organic
alternatives (Mendelsohn et al., 2003). growers, but no insect pests to date have evolved
resistance to transgenic Bt crops in the field
Yield increases of Bt crops compared to (Fox, 2003; Ferry et al., 2006). This has been
conventional varieties have varied depending supported by an eight-year monitoring study
upon the plant species and the geographic (1997-2004) of pink bollworm resistance to Bt
location. In the case of Bt cotton in India, toxin with laboratory assays of strains derived
insecticide applications were reduced 70% annually from 10-17 cotton fields in Arizona.
leading to savings of up to U$ 30 per hectare No net increase in the mean frequency of
in insecticide costs, and an 80-87% increase bollworm resistance to Bt toxin was observed
in harvested cotton in 157 farms (Qaim and (Tabashnik et al., 2005). Likewise, a large-scale
Zilberman, 2003). More than 80% reduction study carried out in Bt corn fields in Spain did
in pesticide applications in Bt cotton fields has not identify any resistant corn borers (Ostrinia
been reported in China, and the proportion of nubilalis and Sesamia nonagrioides) over a
growers with pesticide poisoning was reduced five-year period (Farinós et al., 2004).
Several strategies have been proposed to transgene pyramiding showed that transgenic
maintain durable crop resistance to insects in cotton containing two Bt genes (Cry1Ac and
the field, including a high level of transgene Cry2Ab) performed better than either the single
expression, cultivation of multilines containing gene Cry1Ac or the Cry2Ab transgenic cotton
different insect resistance genes, transgene (Jackson et al., 2004).
pyramiding, cultivation of susceptible plants for
insect refuge, and plant tissue-specific expression The effect of insect-resistant crops on non-
of transgenes (Roush, 1998). An accepted and target insects has been a controversial issue
successful method used in real field conditions related to the use of Bt crops. Scientists at
for preventing the development of resistance to Cornell University reported that the larvae of
Bt crops in insect pests has been the ‘high-dose/ Monarch butterflies fed on milkweed leaves
refuge strategy’, in which the transgene must be covered in pollen from Bt corn grew slower
expressed highly enough to kill almost all of and were smaller than those on control leaves
the susceptible insects. In this case, up to 80% under laboratory conditions (Losey et al.,
of the total area is dedicated to the cultivation 1999). Theoretically, Bt crops should not
of non-Bt crops that are fully susceptible to represent any risk to Monarch larvae, since
the insect pests, depending upon the region, they feed only on milkweed leaves (Slater et
the type of Bt gene, and other transgenic crops al., 2003). However, there is the potential for
grown in the region. The refuge plants serve to the larvae to come into contact with GM corn
maintain a population of the pest that does not pollen that spreads to milkweed surrounding Bt
carry any resistance mutations and can ‘dilute corn fields. The paper sparked off considerable
out’ a potential resistance allele (Christou et public concern in the USA. A major research
al., 2006). However, there is scientific evidence collaboration between six groups in the USA
that argues against the need of refuges in the and Canada studied the Bt pollen toxicity in
context of resistance management (Gressel, more detail, and investigated the likelihood
2005), whereas more recent data corroborates of exposure of monarch caterpillars to Bt
the overall effectiveness of the refuges to delay corn pollen under natural conditions (Sears
resistance (Tabashnik et al., 2008). Failure et al., 2001). This two-year study concluded
to adhere strictly to the refuge strategy for that the impact of Bt corn pollen from current
resistance management, which is likely to occur commercial hybrids on Monarch butterfly
with less controlled and more widespread use populations was very low. Moreover, a meta-
of transgenic crops, will not necessarily lead to analysis of 42 field experiments indicated that
rapid breakdown in the usefulness of Bt crops. non-target invertebrates were generally more
Studies have shown pollen-mediated gene flow abundant in Bt cotton and Bt corn fields than in
up to 31 m from Bt corn that caused low to non-transgenic fields managed with insecticides
moderate Bt toxin levels in kernels of non-Bt (Marvier et al., 2007). Since Bt-transgenic
corn refuge plants (Chilcutt and Tabashnik, varieties can lead to substantial reductions
2004). The authors of the study suggested that in insecticide use under growing conditions,
guidelines should be revised in order to reduce Bt crops can contribute to integrated pest
gene flow between Bt crops and refuge plants. management systems with a strong biological
control component (Romeis et al., 2006).
The expression of two dissimilar Bt toxin genes
represents another effective strategy to delay Virus resistance
the development of resistant insect (‘transgene
pyramiding’) (Roush, 1998). The simultaneous Abel et al. (1986) reported that transgenic to-
introduction of three genes expressing bacco expressing the coat protein (CP) gene of
insecticidal proteins (Cry1Ac, Cry2A, and Tobacco mosaic virus (TMV) was resistant to
Gna) into rice to control three major pests (rice TMV, which spurred the development of virus-
leaf folder, yellow stemborer and the brown resistant transgenic crops. Since then, the initial
planthopper) imparted more resistance than hope that pathogen-derived resistance (Sanford
combinations of only two of these transgenes and Johnson, 1985) might be a practical way to
(Bano-Maqbool et al., 2001). Another study of control plant viruses has been firmly established
and applied to many viruses and crops (Beachy, or environmental risks have been reported. An
1997). Efficient protocols have resulted from ongoing research priority is the assessment of
technical improvements in transgene engineer- risks related to potential gene flow from virus-
ing, in transformation of a variety of crops, resistant GM crops to wild relatives (Fuchs and
and in the understanding of the mechanisms of Gonsalves, 2007). For example, the movement
resistance. However, the commercial potential of transgenes from a virus-resistant transgenic
has not yet been realized since only three virus- squash to its wild relative, Cucurbita pepo
resistant crops have reached the marketplace in spp. ovifera var. texana, was documented in
the USA (Gonsalves et al., 2006). experimental field settings (Fuchs et al., 2004).
One approach for achieving virus resistance is New developments and trends
based on the phenomenon of cross protection,
in which infection by a mild strain of a virus Duke (2005) predicts an increase in the adoption
induces resistance to subsequent infection by of some existing herbicide-tolerant (HT) crops
a more virulent strain. This phenomenon was worldwide, but not the rapid growth that we have
reproduced constitutively in a GM plant by seen during the first decade of their availability.
expressing a transgene encoding a viral CP, Furthermore, although the public reluctance to
and was used in the papaya industry in Hawaii accept HT crops is not predicted to change in
due to an epidemic of Papaya ringpost virus the near future, their neutral and/or favorable
(PRSV) in the nineties (Gonsalves, 1998; environmental effects seem to be causing a shift
Ferreira et al., 2002). This approach was toward governmental approval of HT crops in
effective in protecting against the severe strains some geographic areas. The introduction of a
of PRSV, but produced severe symptoms on large number of new HT crops over the next 5
certain cultivars, such as ‘Sunrise’, and thus did years is not expected (Duke, 2005).
not receive widespread use (Pitz et al., 1994).
However, one mild strain of PRSV was later Resistance to dicamba has been recently
used as the source of CP for the PRSV-resistant developed (Behrens et al., 2007). Dicamba, an
transgenic papaya currently commercialized in auxin-type herbicide, is a widely used, low-cost,
Hawaii (Gonsalves et al., 2006). environmentally friendly herbicide that does
not persist in soils and shows little or no toxicity
Another approach uses antisense or co- to wildlife and humans (Stevens and Sumner,
suppression techniques, which consist in 1991). Behrens et al. (2007) isolated a bacterial
inserting a complementary version of the target gene, DMO (dicamba monooxygenase), that
gene in an antisense orientation to reduce the encodes a Rieske non-heme monooxygenase.
amount of the viral protein when the virus Transgenic plants expressing DMO are capable
infects a plant. For example, a GM potato virus- of inactivating dicamba. Tobacco, tomato,
resistant variety carrying a replicase gene from soybean, and Arabidopsis plants containing the
Potato leaf role virus (PLRV) in combination DMO gene were fully resistant to treatments
with the Bt insect-resistance trait has been with dicamba at the normal application
engineered. This technology has being applied rates and up to 20 times these levels (i.e., 5.6
to achieve resistance to other plant viruses, kg.ha-1), without significant herbicide damage
such as the resistance to Potato tuber necrotic symptoms. Behrens et al. (2007) speculate
ringspot virus in potatoes (Racman et al., about the potential combination in the future of
2001). Currently, transgene-mediated RNA the dicamba resistance gene with the glyphosate
silencing and generation of small interfering resistance gene in order to allow growers to
RNAs appear to be primary mechanisms that alternate applications between both herbicides
confer resistance to plant viruses (Sudarshana or to use mixtures of the two herbicides
et al., 2006; Prins et al., 2008). together. In either case, appearance of weeds
resistant to either glyphosate or dicamba would
Extensive safety assessment studies have been be greatly suppressed. The possibility of using
carried out over the past 15 years involving virus- two different herbicides before sowing or at a
resistant transgenic plants. Overall, no health variety of time points during crop development
would allow a more flexible weed control. inducible promoters. In this approach, the
Additionally, dicamba-resistant crops would transgenic plant itself can serve as a refuge as
further encourage the use of conservation tillage long as either the expression of the insecticidal
practices with all the positive consequences gene is not induced or the induction wears off
discussed above. (Bates et al., 2005).
The area devoted to growing GM crops Mehlo et al. (2005) engineered plants with
expressing insecticidal Cry proteins derived a fusion protein combining the δ-endotoxin
from Bacillus thruringiensis (Bt) has increased Cry1Ac with the galactose-binding domain of
steadily since their introduction one decade ago the non-toxic ricin B-chain (RB). Transgenic
(Romeis et al., 2006). The most likely tendency rice and corn plants designed to express the
is that new transgenic plants expressing novel fusion protein (BtRB) were significantly more
Cry or other insecticidal proteins, stacked genes toxic in insect bioassays than those containing
or fusion proteins will increase in importance the Bt gene alone, due to increased number of
in the coming years (Bates et al., 2005). Plants potential fusion protein-receptor interactions at
might be introduced in the future that express the molecular level in target insects.
multiple novel insecticidal proteins, such as the
Vip (vegetative insecticidal proteins) produced Transgenic plants overexpressing protease in-
by Bacillus thuringiensis during its vegetative hibitors (PIs) that affect the insect digestive
growth, imparting a wider spectrum of pest system have to date shown marginal effective-
control (Yu et al., 1997; de Maagd et al., 2003). ness against insect pests (Christou et al., 2006).
However, the use of novel inhibitors, such as the
The use of synergists has become one strategy barley trypsin inhibitor (Alfonso-Rubi et al.,
to increase Bt Cry protein toxicity and to 2003), synthetic constructs containing multiple
overcome and delay insect resistance to this inhibitors (Outchkourov et al., 2004), equistatin
biopesticide (Tabashnik, 1994). For example, from sea anemone (Gruden et al., 1998), other
a fragment of a toxin-binding cadherin (CR12- cystatins (Martínez et al., 2005), and lectins
MPED peptide) has the potential to increase (Zhu-Salzman et al., 2003) might prove useful.
the control of lepidopteran pests by Cry1A
toxins. This synergist is a good candidate for Triple-stack traits (dual Bt genes combined with
development of a more effective strategy to glyphosate or glufosinate resistance) are likely
control Lepidopteran pests that are presently not to replace many of the single-trait products
being efficiently controlled by Bt crops, such as (Castle et al., 2006). However, this poses
the case of cotton bollworm (Helicoverpa zea) the challenge of how multiple genes can be
(Chen et al., 2007). transferred into the same plant genome, giving
rise to technical and regulatory limitations. One
Other non-conventional sources for insect possibility for overcoming these restrictions is to
resistance are Photorhabdus and Xenorhabdus focus on the plant plastome, i.e., the chloroplast
bacteria, which are symbionts of certain types genome. Engineering the plastome represents
of nematodes. They cause lethal septicemia in an exciting development of modern plant
the insect, whose tissues are used as nutrients biotechnology (Daniell and Dhingra, 2002;
by the nematode (Chattopadhyay et al., 2004). Slater et al., 2003; Svab and Maliga, 2007).
Considerable progress has been made in the First, chloroplast genes are, like prokaryotic
identification of several toxin genes from these genes, often found in operons, where one
two bacteria (Williamson and Kaya, 2003). promoter regulates the expression of a group
of genes. Therefore, a group of foreign genes,
Although constitutive expression of insecticidal organized in an operon, can be introduced
transgenes has provided high levels of resistance under the control of a single promoter. There
in crop plants, tissue-specific or inducible are several important advantages associated
expression might be desirable under some with plastome transformation: (i) all the genes
circumstances. For instance, the novel strategy are expressed at similar levels; (ii) high levels
‘within-plant refuge’ has been developed using of transgene expression and foreign protein
accumulation are relatively common with and Russell, 2002). Vitamin A deficiency, a
chloroplast transformation, thanks to the major problem in parts of the developing world,
co-existence of multiple copies of genomes can result in permanent blindness and increased
(>50) per chloroplast and the presence of 50 susceptibility to infectious diseases (West and
or more chloroplasts per plant cell; (iii) gene Darnton-Hill, 2001). Since no rice cultivars
silencing does not seem to be a problem; (iv) produce provitamin A in the endosperm,
homologous recombination allows transgenes recombinant technologies related to GM crops,
to be inserted precisely into the chloroplast rather that conventional plant breeding, were
genome; (v) antibiotic resistance genes do not required to engineer rice with β-carotene,
need to be used as selectable markers or they called ‘Golden Rice’ (Ye et al., 2000). Three
can be easily excised (Daniell et al., 2001); (vi) genes were used (i.e., psy, lcy from daffodil and
cytotoxicity of the foreign protein seems to be crtI from bacteria) to enable the biosynthesis
less a problem than with nuclear transformation of provitamin A in the endosperm of GM rice.
(Slater et al., 2003). Although the technology However, the work was somewhat limited by the
to obtain marker-free transplastomic plants low levels of carotenoids accumulated (1.6 µg·g-1
is available, no transplastomic crops are yet carotenoid in the endosperm). Paine et al. (2005)
grown commercially. One reason is slow hypothesized that the daffodil gene encoding
implementation of the tissue culture-based phytoene synthase (psy) was the limiting step in
plastid transformation technology outside the β-carotene accumulation. Through systematic
group of Solanaceous species, although recently testing of other plant psy genes, they identified
genetically stable transplastomic variants have a psy from corn that considerably increased
been obtained in a diverse group of species, carotenoid accumulation in a model plant
including cauliflower, cotton, soybean, lettuce, system. When expressed in rice, this ‘Golden
and poplar. The cereal crops wheat, corn Rice 2’ accumulated total carotenoids of up
and rice continue to be recalcitrant to plastid to 37 µg·g-1, or a 23-fold increase compared
transformation (Lutz and Maliga, 2007). to the original Golden Rice. This translates to
delivering 50% of the children’s Recommended
Apart from herbicide-tolerant and insect- Daily Allowance (RDA) in 72 g of dry new
resistant GM crops, other genetically engineered ‘Golden Rice 2’ (Paine et al., 2005). Recently,
agronomic traits are currently being developed, the accumulation of carotenoids was further
such as fungal resistance (Rommens and Kishore, increased and engineered in GM potatoes
2000; Dangl and Jones, 2001; Mondal et al., (‘Golden potatoes’). Assuming a β-carotene to
2007; Ohsato et al., 2007), drought tolerance retinol conversion of 6:1, this newly developed
(Shou et al., 2004; Dezar et al., 2005; Brini et GM crop is sufficient to provide 50% of the
al., 2007), salt tolerance (Zhang and Blumwald, RDA of vitamin A with 250 g (fresh weight) of
2001; Zhang et al., 2001; Flowers, 2004; Brini et ‘golden potatoes’ (Diretto et al., 2007).
al., 2007), and nematode resistance (Williamson,
1998; Huang et al., 2006). Genetic engineering of new storage oils and
fats has produced oil crop plants with fatty acid
Another exciting field of modern plant biotech- compositions, many of which are unattainable
nology is represented by the enhancement of crop or difficult to obtain by plant breeding alone.
nutritional properties through genetic modifica- The combination of classical breeding methods
tion (Rein and Herbers, 2006). There are multiple with molecular techniques provides new ways
nutritional advances underway and this review for designing oils for food and industrial uses.
focuses on two representative examples that illus- Alterations in the position and number of
trate the potential impact of this technology. carbon double bonds, variation in fatty acid
chain length, and the introduction of desired
Carotenoids are a group of plant pigments functional groups have already been achieved
important in the human diet that serve as the only in model systems (Töpfer et al., 1995). For
precursors of vitamin A. Some carotenoids, most example, lauric acid (12:0), which is used in
importantly β-carotene, are cleaved to vitamin a variety of cosmetics and other products, is
A and are referred to as provitamin A (Yeum derived primarily from palm and coconut oil.
However, by inserting into rapeseed a specific effectiveness of the herbicide has stimulated
lauroyl-ACP thioesterase gene derived from seed companies to engineer glyphosate-
the bay tree, scientists at Calgene were able to resistant crops and convinced growers to grow
increase lauric acid production to around 40% them. They have had remarkable ecological
of the total fatty acids, compared with 0.1% and environmental impact in diminishing soil
in unmodified oilseed rape (Halford, 2006). erosion due to reduced cultivation or non-tillage
Similarly, Calgene scientists were able to block practices. The model has proven so successful
the activity of a desaturase in rapeseed that that of the transgenic crops planted worldwide in
converts stearic acid (18:0) to oleic acid (18:1), 2006, approximately 80% were engineered to be
resulting in a high-stearic acid oil useful in glyphosate-resistant. Nevertheless, this success
margarines. In addition, there is considerable could become a potential failure if modern
potential in the production of a very high agriculture becomes too dependent on a single
(>90%) oleic acid oil for food purposes and as chemical. Some researchers have stated that
uniform oleochemical feed-stock. Conventional “glyphosate is as important to world agriculture
breeding has produced mutant oilseed rape as penicillin is to human health” (Service, 2007).
lines with oleic acid content close to 80%, but The comparison is valid because pathogens
attempts to increase this level have resulted in have grown resistant to penicillin and other
plants with poor cold tolerance, presumably as antibiotics, and resistance to glyphosate will
a result of the lack of unsaturated fatty acids likely result in an increased appearance of weed
in their cellular membranes. Antisense and co- resistant biotypes in different production areas,
suppression techniques to reduce expression of according to several experts (Service, 2007).
a specific desaturase in the seeds of GM oilseed To preserve the effectiveness of glyphosate as
rape have, however, raised the oleic acid levels long as possible, several resistance management
up to 88%, without affecting cold tolerance strategies have been proposed by weed
(Slater et al., 2003). Similar experiments in specialists. Among these are rotating crops and
soybean seeds by DuPont increased the oleic using a variety of different herbicides to control
acid level from 20% (non-GM soybean) to weeds, practices that hinder resistant organisms
80% (GM soybean) (Halford, 2006). Another from gaining a foothold in the growers’ fields.
example that is nearing commercialization is In practice, this means rotating crops that do
the development of omega-3 fatty acids derived not rely on using glyphosate. Another strategy
from GM crops. They provide the health- is to use GM crops resistant to other herbicides,
beneficial effects of long-chain polyunsaturated such as glufosinate. These GM crops have
fatty acids found in fish oils (Graham et al., not done as well in the market as glyphosate-
2007). These genetically engineered oils resistant crops (GRCs) probably because the
were developed since oil-seed species do herbicide is more expensive and less effective
not synthesize these products naturally and at killing a broad range of weeds. Dicamba,
because of the significant reduction in fish oil another inexpensive herbicide that has been on
consumption in recent years (Qi et al., 2004). the market for four decades, could emerge as a
complement to glyphosate. If so, this will allow
Discussion and conclusions growers to rotate their crops between varieties
resistant to at least two different herbicides,
This article has mainly focused on the giving farmers an alternative to the continual
importance of HT crops and Bt crops since use of GRCs, which would considerably delay
these two transgenic technologies cover almost the appearance of weeds resistant to glyphosate.
all the global area cultivated with GM crops. Another approach is to combine, or ‘stack’,
Over the past 12 years, biotech crop area has genes for resistance to multiple herbicides in
increased more than 67-fold, making GM the same plant. According to Nicholas Duck, a
crops one of the most rapidly adopted farming crop scientist in North Carolina, “in the future,
technologies in modern history (James, 2007). everything is going toward product stacks”
Glyphosate is the world’s most used herbicide (Service, 2007). For example, Pioneer Hi-Bred
due to its safety and effectiveness at controlling (DuPont) recently engineered HT soybean
hundreds of different kinds of weeds. The and HT corn with higher levels of glyphosate
resistance in addition to sulfonylurea resistance they will not interbreed with USA wild species.
(Pioneer Hi-Bred, 2007). One question that A reasonable concern exists in geographic
arises is whether crops resistant to multiple locations where there is the potential for
herbicides will prolong the useful life of transmission of genes to wild relatives (i.e., corn
glyphosate. Another question is whether all in Mexico, rice in China). A more immediate
the approaches described above to preserve the problem is gene flow from herbicide-resistant
effectiveness of glyphosate will be followed crops to non-transgenic crops of the same
by growers in developing countries, where the species. This has already been reported in
protocols of resistance management are usually North America in crops (i.e., canola, rice, and
less rigid than in developed countries. creeping bentgrass) that were meant to be kept
transgenic free, and there is a need for technology
A concern associated with the use of HT crops to prevent introgression from transgenic crops.
is the potential introgression of genes from GM There are several approaches for mitigation or
crops into wild relatives (i.e. gene flow) and the elimination of introgression of transgenes: (A)
potential impact of this on natural ecosystems. Use sterile varieties. For example, Webster
For gene flow to take place among cultivars and et al. (2003) recommended triploid, non-
their wild relatives, several barriers have to be pollen producing or -receiving cultivars of
overcome, including the presence of cultivars bermudagrass for introduction of herbicide-
or wild relatives within pollen or seed dispersal tolerant turf. (B) Utilize isolation requirements
range, the ability to produce viable and fertile for achieving transgene confinement depending
hybrids, at least partial overlap in flowering on the type and the pollinator activity. For
time, actual gene flow by pollen or seed, and the example, non-GM rice showed marked
establishment of crop genes in the domesticated reductions in transgene flow with short spatial
or wild recipient populations (Gepts and Papa, isolation (i.e., 6.2 m) from GM rice (Rong et
2003). Other aspects that affect gene flow are al., 2007). Pollen-mediated gene flow (PGF)
the type of transgene, its insertion site, the decreased exponentially with distance from HT
density of plants and ecological factors (Felber cotton and low levels of PGF (i.e., <0.5%) were
et al., 2007). A persuasive argument can be detected at 30 m (Van Deynze et al., 2005),
made that an herbicide resistance gene should and 1.5 km from HT alfalfa (Van Deynze et
have no fitness advantage in a natural habitat al., 2004) when pollinated by honeybees. (C)
where the herbicide is not used (Stewart et al., Transformation of the chloroplast genome would
2003), and glyphosate resistance might reduce prevent or greatly reduce gene flow through
fitness under non-agricultural conditions pollen flow (Daniell et al., 1998). Chloroplasts
(Baucom and Mauricio, 2004), depending are normally inherited maternally, in the same
upon the mechanism of resistance. However, in way that organelles such as mitochondria are
contrast with domestication genes, which often in animals. This predominantly maternal
make crops less adapted to natural ecosystems, inheritance has two beneficial effects. First,
transgenes frequently represent gain of function, gene transfer to weedy relatives, which occurs
which might release wild relatives from principally through pollen, is reduced. Second,
constraints that limit their fitness (Gepts and pollen from plants in which the chloroplast
Papa, 2003). Transgenes that might increase the genome has been transformed does not
fitness and competitiveness of wild relatives of represent a toxic risk to non-target species
crops in natural ecosystems include those that (i.e., the ‘Monarch butterfly’ controversy), as
confer insect and disease resistance, drought the detection of paternal plastid transmission
and salt tolerance, which could be important in occurs very rarely under field conditions (Svab
natural habitats (Stewart et al., 2003). and Maliga, 2007). This has proved to be the
case even when the transgene product normally
Cotton and corn with transgenes encoding accumulates to a very high level (Slater et al.,
both insect and herbicide resistance have been 2003). The plastid transformation technology
approved for commercialization in the USA. looks promising since Monsanto licensed it,
However, introgression is not a concern for and it could be commercially available with
these two crops in most of the country because 3 to 4 years (Service, 2007). However, this
technology will likely not solve by itself all the troduction of GM crops in those markets where
introgression problems derived from the use of people are reluctant to accept and incorporate
GM crops. Other approaches for reducing gene this technology, particularly in the European
flow have also been documented (Stewart et al., Union. Social, economic and political reasons
2003; Cerdeira and Duke, 2006; Gressel, 2007). explain this rejection of transgenic crops that go
Combining effective and widespread methods beyond the scope of this article. It is possible that
for eliminating gene flow is an important step for the public opinion could change if the benefits of
preventing the potential environmental impact of GM crops were more tangible. All the GM crops
transgenic crops, and consequently, increasing presently available in the market are traits that
the success of GM crops in the future. benefit the farmers (‘input traits’), but none of
them are benefiting the consumer directly (‘out-
The advantages of insect-resistant transgenic put traits’). The classic example of ‘output trait’
plants (Bt crops) have been reviewed in this is the case of ‘Golden Rice’. This product started
article. Overall, Bt crops reduced insecticide to be developed in 1992 and is expected to be
usage in the USA by 3,700 tons in 2005, providing commercially released in 2011 in the Philippines
benefits for human health and the environment and India (Mayer, 2007). From the humanitarian
(Sankula, 2006). Yields of Bt cotton and Bt corn prospective, this 20-year wait for the release of
have been increased, especially in developing ‘Golden Rice’ has been harmful if we consider
countries. The report that Monarch butterfly that 124 million children are deficient in vitamin
larvae were killed after eating pollen from corn A (Humphrey et al., 1992), and that improved
plants expressing the Bt toxin had great impact nutrition in vitamin A could prevent 1 to 2 mil-
on public opinion (Losey et al. 1999). However, lion deaths annually (West et al., 1989). An ini-
subsequent field trials indicated that while this is tial obstacle to the delivery of ‘Golden Rice’ to
true in laboratory tests, exposure of the larvae to its potential beneficiaries was the protection of
the transgenic pollen is quite low in the natural intellectual property rights (IPRs), with 70 IPRs
environment (Sears et al., 2001). The risk to and technology protection rights belonging to
non-target insects from Bt pollen is much less 32 different companies and universities (Slater
than that from insecticides that would be used et al., 2003). However, in practice this obstacle
if the crop did not contain the Bt trait (Pimentel was readily overcome with licensing agreements
and Raven, 2000). Overall, Bt crops showed that allowed the humanitarian use of the relevant
less detrimental effects on non-target species IPRs in developing countries. The major delay
than using conventional insecticides on non- in deployment of ‘Golden Rice’ has been due to
transgenic crops (Marvier et al., 2007). Second- the regulatory system that required complete re-
generation techniques were launched to the design of the vectors used, the identification of
market in 2003 and have limited the expression only a single transgenic event to deregulate, and
of the Bt protein only to the leaves, stem or the exhaustive testing that is required only of
roots, eliminating the toxin protein from pollen. transgenic crops (Mayer, 2007). The regulatory
Since there is no insect pest that has developed system and particularly the Cartagena Protocol
resistance to Bt crops to date, it appears that the on Biosafety and the Convention on Biological
practices developed to delay resistance of pest Diversity is making very restrictive rules based
insects to Bt crops (i.e., high expression levels, upon the ‘precautionary principle’ that results in
refuges and transgene pyramiding, among considerable hurdles for international trade in
others) have been successful. It is likely that biotechnology crops (De Greef, 2004), where
these resistance strategies will be improved the only trigger is whether recombinant DNA
in the future, as well as new transgenic plants techniques are employed. Identical traits devel-
expressing novel Cry or other insecticidal oped by ‘traditional’ techniques (i.e., mutation
proteins, use of synergists and insect digestion or breeding) do not encounter such hurdles, even
inhibitors, stacked genes, and fusion proteins though they may have comparable environmen-
will increase the toxicity and selectivity of Bt tal impacts. A sensible approach would be to
toxins to control the target insects. deregulate biotechnology traits in proportion to
their potential risk and in light of experience with
Public acceptance is a key issue for further in- both traditional and biotechnology methods of
genetic improvement (Bradford, 2007; Bradford to their benefits, and compare them with the
et al., 2005). The potential benefits of agricultur- traditional methods of genetic improvement.
al biotechnology, such as improving nutritional
quality or reducing pesticide use, are too great Resumen
to be withheld from the majority of the world’s
population due to regulatory issues. As Nobel Los cultivos genéticamente modificados (GM)
Peace Price recipient Dr. Norman Borlaug noted fueron introducidos a mediados de los noventa y
(Borlaug, 1997), “this issue goes far beyond eco- hay actualmente dos tecnologías principales de
nomics and regulatory issues; it is also a matter transgénicos en el mercado, los cultivos tolerantes
for deep ethical consideration. Fundamentally, a los herbicidas (HT) y los cultivos resistentes a
the issue is whether small-scale farmers of the insectos (cultivos Bacillus thuringiensis (Bt)).
developing world also have a right to share in the Los cultivos HT han simplificado y reducido los
benefits of biotechnology. If the answer is yes, costos de manejo de malezas a los productores
then what is the role of international and national y han favorecido el medio ambiente. Sin
governments to ensure that this right is met? I be- embargo, existe inquietud por el desarrollo
lieve we must give this matter serious thought”. potencial de malezas resistentes al glifosato,
The Public Research and Regulation Foundation el principal herbicida empleado en cultivos
has been established to provide an avenue for HT. Una segunda trascendental preocupación
input from public researchers into the interna- asociada al uso de cultivos HT es la introgresión
tional biotechnology regulatory process (www. potencial de genes desde los cultivos GM a las
pubresreg.org). Seed biotechnology researchers especies cercanas nativas (flujo génico) y su
who hope to see the results of their efforts trans- impacto en los ecosistemas. Los cultivos Bt han
lated into agricultural practice are encouraged to incrementado los rendimientos, reducido el uso
become engaged in this process so that sensible de insecticidas, lo que ha consiguientemente
regulatory protocols can guide the safe applica- beneficiado la salud de los productores y el
tion of seed biotechnology for agricultural and ambiente. Sin embargo, el desarrollo potencial
consumer benefit (Bradford, 2007). de resistencia de los insectos a las toxinas
Bt y el daño indirecto de las toxinas Bt a
Finally, genetic engineering should not be especies no albo a éstas constituyen problemas
considered as the ‘silver bullet’ that will solve relevantes relacionados al uso de cultivos Bt.
all the problems of growers and the worldwide Diferentes estrategias para mitigar y eliminar
human malnutrition. Instead, it should be los problemas asociados al uso de transgénicos
regarded as a very powerful tool that will son discutidas en el artículo. La próxima etapa
complement traditional plant breeding. It is en biotecnología vegetal es la introducción de
expected that ‘realistic’ predictive models and semillas mejoradas en su composición nutritiva,
risk assessment for evaluating GM crops in lo que va a beneficiar a los consumidores
both laboratory and field conditions will be directamente.
fine tuned in the future in order to optimize
benefits and time while reducing potential Palabras clave: Cultivos Bt, flujo génico,
risks. The introduction of GM crops should cultivos genéticamente modificados, glifosato,
be critically analyzed ‘case by case’ due to the Arroz Dorado, cultivos tolerantes a herbicidas,
complexity of the biological issues and to avoid cultivos transgénicos.
irreversible damage to ecosystems, especially
by gene flow. In order to determine the impact Acknowledgements
of the introduction of a GM crop, benefits and
risks should be carefully analyzed in each case The author thanks the Western Regional Seed
and compared to those associated with current Physiology Research Group, a group of seed
practices. However, the current international companies that support research at UC Davis,
regulatory system of GM crops is based on the for funding. I am very grateful of Kent J.
‘precautionary principle’ that only considers Bradford, Dario Cantu, and Cristóbal Uauy, for
the risks of using GM crops. Instead, it should their constructive comments on the manuscript.
evaluate the risks of utilizing GM crops relative
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An update on genetically modiﬁed crops

Article in Ciencia e Investigación Agraria · December 2008

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An update on genetically modified crops

Introduction An important breakthrough in the development

Table 1. Examples of commercially available genetically modified crops.

Crop Trait Target Trait Originating Year of first Trade

Million hectares, 1996-2007

target plants represents a direct environmental

References Carpenter, J., A. Felsot, T. Goode, and M. Hamming.

enhanced drought tolerance in transgenic as determinants of the specificity of Bacillus

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