Genetically Modified Plants: Assessing Safety and Managing Risk

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Preface

For over 10,000 years, humans have tried to control their food supply through agriculture, moving from being hunter-gathers to selecting and improving wild species of plants and animals. Thanks to continuous progress in plant breeding, agriculture has managed to meet the needs of ever-increasing human populations in essential food crops, as well as addressing the challenges of abiotic and biotic constraints in crop production. However, food security faces growing challenges in light of demographic and climate changes. Modern advanced plant breeding is likely to address some of the future food needs, but the lack of useful traits in sexually compatible plant species sets an upper limit to what can be achieved by breeding techniques. This limitation can be overcome by the ability to manipulate plant genomes through genetic engineering. The adoption of genetically modified (GM) plants in agriculture has triggered new regulations requiring their safety assessment, as well as that of derivative products, before their environmental release and commercialization. Regulations regarding genetically modified organisms (GMOs) have played a critical role not only in the commercialization of GM crops but also in research and development.

Since the first edition of this book, we have witnessed phenomenal advances in plant sciences and the emergence of a new range of GM techniques spearheaded by genome editing. These advances could bring a paradigm shift in crop improvement. Genome-editing techniques allow the elucidation of complex genomic networks and the modification of plant genomes with increasing precision and predictability. The application of these techniques raises the question whether the regulatory threshold for the commercialization of genome-edited plants should be the same as with GMOs or reduced. This new edition reviews current and anticipated future applications of GM technology, provides background on GMO regulation, and critically analyzes differences among different regulatory systems.

Chapters 1–3 set the scene with descriptions of the constraints affecting crop production, and the range of available and emerging technologies that can be used to address these constraints. Chapter 1 provides a general introduction to agricultural systems and constraints on crop production due to abiotic and biotic stresses, particularly in light of climate change and population demographics. Chapter 2 deals with classical and advanced plant breeding, and genetic modification techniques including genome editing. Chapter 3 gives an overview of the adoption of GM crops in terms of crop-trait combinations and describes current applications of genome editing in plants.

The main body of the book comprises five chapters analyzing various aspects of risk assessment, regulatory systems, and how potential risks are managed. Chapters 4 and 5 go into details of the concepts of hazards and risk, how GM-plant risks are assessed and managed, and international and national regulatory systems. The concepts of the regulatory trigger, the product/process approaches to risk assessment, and the precautionary principle are explained. These chapters place particular focus on the baselines against which risk assessment is made, and grey areas in risk assessment procedures. The next three chapters describe the types of information needed and the questions asked in assessing the potential risks related to environmental releases and consumption of GM crops and derivative products. Chapter 6 covers the molecular characterization of GM plants in terms of transformation methods used, the introduced DNA, and the phenotypic characteristics of the final product. Chapter 7 describes the specific risk assessment procedures that are applied to GM plants intended for human consumption or animal feed. Risk assessment procedures for GM plants released into the environment are covered in Chapter 8.

Chapter 9 provides an overview of issues affecting the public acceptance of GM plants and products thereof. The last chapter deals with medium- and long-term issues that may impinge on regulatory structures in the future. Several appendices providing supporting information follow these chapters.

This book is aimed at professionals in government and industry dealing with GMO regulatory affairs, researchers involved in the development of GM plants, undergraduate and graduate students in plant sciences, and all those wishing to be informed on the subject.

Chapter 1: Setting the context: Agriculture and crop/food sustainability

Abstract

This chapter describes the history of agriculture and constraints on crop production, including the potential effects that climate change and population increase will have over the next few decades. By highlighting the constraints on crop production, it sets the scene for the need for new technologies, especially genetic modification and other molecular DNA techniques, to help mitigate them, and provides the background for the risk assessment and management topics described in subsequent chapters.

Keywords

History of agriculture; Constraints on crop production; Abiotic constraints; Biotic constraints; Climate change; Food sustainability

Chapter Outline

1.History of crop production

1.1Development of modern crop production

1.2Agricultural systems

2.Abiotic and biotic constraints on crop production

2.1Abiotic constraints

2.2Biotic constraints

2.3Interactions between abiotic and biotic stresses

3.Other constraints: Food security and sustainability

3.1Population demographics

3.2Social and cultural considerations

3.3Policy and economic considerations

4.Conclusions

References

1: History of crop production

1.1: Development of modern crop production

a

Crop production is generally considered to have started during the Neolithic Period when humans moved from being hunter/gathers toward organized societies with food producers and food consumers, though some evidence is emerging of small-scale crop production at least 11 millennia earlier in the Paleolithic Period (Snir et al., 2015). Suitable wild plant species were domesticated by choosing those variants that had desirable properties (e.g., yield, reliability, lack of toxins, and ease of cultivation). Crop production originated in the primary centers of origin of the plant species (Box 1.1) being domesticated.

Box 1.1

Centers of origin of crops

The early domestication of crops occurred in their centers of origin. Vavilov (1935) identified eight primary centers of origin of most of the world’s crops (Box 1.1 Figure 1):

Box 1.1 Figure 1 Vavilov’s (1935) primary centers of origin of the world’s major crops.

I    The Chinese Centre is the center for crop species that include rice, buckwheat, soybean, Chinese yam, radish, Chinese cabbage, onion, cucumber, pear, peach, apricot, cherry, walnut, sugarcane, and hemp.

IIa    The Indian Centre is the center for crop species such as rice, chickpea, cowpea, eggplant, cucumber radish, taro, yam, mango, orange, sugarcane, coconut palm, sesame, black pepper, and bamboo.

IIb    The Indo-Malayan Centre is the center for crop species that include velvet bean, banana, mangosteen, coconut palm, sugarcane, and black pepper.

III    The Inner Asiatic Centre is the center for crop species that include wheat, pea, lentil, horse bean chickpea, mustard, flax, cotton, onion, garlic, carrot, pear, almond, grape, and apple.

IV    The Asia Minor or Near-Eastern Centre (also known as the Fertile Crescent) is the center for crop species that include wheat (einkorn, durum and common), rye, oats, lentil, lupine, alfalfa, fig, apple, pear, and cherry.

V    The Mediterranean Centre includes crop species such as durum wheat, emmer, spelt, pea, lupin, various clovers, flax, oilseed rape, olive, beet, cabbage, turnip, lettuce, parsnip, and hop.

VI    The Abyssinian (now Ethiopian) Centre contains crop species such as emmer, barley, pearl millet, cowpea, flax, and coffee.

VII    The South Mexican and Central American Centre contains crop species such as maize, common bean, lima bean, winter pumpkin, sweet potato, papaya, cherry, tomato and cacao.

VIII    The South Andes region comprises three centers:

VIIIa    Peruvian, Ecuadorian, Bolivian Centre contains crop species that include various potato species, lima bean, common bean, tomato, pumpkin, Egyptian cotton and tobacco.

VIIIb    The Chilean Centre contains crop species that include common potato and wild strawberry

VIIIc    The Brazilian-Paraguayan Centre is important for manioc (cassava), peanut, rubber tree, pineapple, and Brazil nut.

The major crop domestications were in the Fertile Crescent (IV) about 11,000 years before present (BP), at least three separate domestications of rice in China (I) and India (IIa) (c.13,500–9000 BP) (Civáñ et al., 2015), domestication and selection of a natural hybrid of 2 species of Musa (banana) in India (IIa) (c.5000–4000 BP) and the New Guinea Highlands (IIb) (c.5000–c4000 BP), and sub-Saharan Africa (not in the Vavlov list) (5000 to c.4000 BP) (coffee, sorghum, oil palm).

While the primary domestication of the various crops occurred in these centers of origin, there are various other centers of secondary diversification. For instance, banana has been further diversified in the Indo-Malayan region, in East Africa and in West Africa.

The centers of origin and diversification are important sources for genes for plant breeding as they contain the wild species and landraces used by indigenous farmers. There can be specific biosafety considerations for the release of GM crops in these regions.

Over a long period of time, farmers practiced empirical crop breeding by selecting the best variants, cross-fertilizing them, and then further selecting the best of the offspring. This form of crop breeding could only be done on locally available varieties and species, and so initial advances in the properties of each crop were associated with the centers of origin. These newly domesticated and improved crops were then spread regionally through the movement of people (e.g., migration, conquest, exploration) and attempts were made to adapt some of them to local environments leading to populations of crop species known as landraces. With increasing intercontinental trade, crops were dispersed worldwide to other climatic areas where they could be grown.

1.2: Agricultural systems

Over the last 200 years or so, increases in human population and urbanization have led to agriculture dividing more markedly between rural food producers and urban populations which rely on these producers for food. These and other factors have resulted in a requirement for increased and consistent food supplies, with concomitant changes in agricultural practices and stronger recognition of the constraints on crop production.

The total world land area is about 13.4 billion hectares (blnha), of which the Food and Agriculture Organization (FAO) classifies about 37% (4.9 blnha) as agricultural area and about 11% (1.5 blnha) as used for crop production. There are estimated to be more than 570 million farms worldwide of which more than 80% are classified as small farms (less than 2.2 ha) (FAO, 2014; Grain, 2014; Lowder et al., 2016). The majority of small farms are in Africa and Asia, with a relatively small proportion in Europe and North America.

Essentially agriculture involves the capture of solar energy to give a range of products that are used for human food, animal feed and, more recently, industrial processes such as the production of ethanol and medicinal products. Animals are also fed by grazing, which uses a further 22% of the world land area. Thus food and feed involve about 1/3 of the global land area. The proportion of crop production used for food versus feed varies among different societies, with the more affluent having diets containing more animal products. Another source of animal feed is crop products (particularly from corn and soybeans), and consequently, more affluent societies use more crop products per capita because the conversion of plant products to animal products is relatively inefficient (Box 1.2).

Box 1.2

Feed conversion ratios

In animal husbandry, the feed conversion ratio (FCR) measures the efficiency with which livestock animals convert feed into the desired output. It is calculated by dividing the mass of input by the mass of output and is a function of the animal’s genetics, its age, the quality and ingredients of the feed, and the conditions under which the animal is kept.

Thus requirements for crop production increase not only with population size but also with the affluence of societies. As well as crop production, humans cultivate trees (silviculture or forestry) and fish (aquaculture), both of which are seeing applications of modern biotechnology.

The most common ways of categorizing types of crop and animal farming are shown in Fig. 1.1.

Fig. 1.1 (A) World distribution of farming types. (B) Agriculture and forest land 2005: Proportions of the total 8950 million ha. Panel (A): Modified from https://geography-revision.co.uk/gcse/agriculture/distribution-of-farming-types . Panel (B): Kampman et al. (2008).

The two basic types of crop production are commercial farming and subsistence farming, although these do increasingly overlap. Commercial (grain and seed) farming (also called commodity crop farming) generally involves growing a single crop species (monocultures) over large areas. It usually uses annual species (e.g., cereals, oilseed rape, soybean, cotton) with annual harvests. Perennial crops (e.g., tea, coffee, bananas, oil palm, and commercial forests) are also grown in large areas in plantations with harvesting over several (or many) years. The main aim of commercial agriculture is to provide (sell) human food (mainly for urban areas and trade) and animal feed, with profits for the farmer. This type of farming also includes pastures with various inputs for feeding animals. Subsistence farming is growing a mixture of food and feed crops for the farmer’s family on small areas of land, with any excess sold locally; subsistence farming makes up the majority of small farms mentioned earlier. Other terms to describe farming types are extensive where there are minimum inputs (e.g., cash, fertilizers, crop protection products) and intensive where there are high levels of inputs (e.g., fertilizers, crop protection products, irrigation, mechanization). Some of the features of intensive commercial and basic subsistence farming are presented in Table 1.1, though it must be emphasized that overall farming systems are moving from subsistence to commercial in many countries.

Table 1.1

Waddington et al. (2010).

Sources of data (year):

a https://www.statista.com/statistics/196106/average-size-of-farms-in-the-us-since-2000/ (2017).

b https://www.statista.com/statistics/196103/number-of-farms-in-the-us-since-2000/ (2017).

c https://en.wikipedia.org/wiki/Agriculture_in_the_United_States (2008).

d https://www.farmflavor.com/at-home/cooking/farm-facts-the-united-states-farmer/ (2012).

e https://www150.statcan.gc.ca/n1/pub/95-640-x/2011001/p1/p1-01-eng.htm (2011).

f https://en.wikipedia.org/wiki/Agriculture_in_Canada (2001).

g https://www150.statcan.gc.ca/n1/daily-quotidien/180831/dq180831b-eng.htm.

h https://www.graincentral.com/cropping/fewer-larger-farms-as-consolidation-continues-in-australian-grain-industry/ (2017).

i https://www.nff.org.au/farm-facts.html (2017).

j https://ec.europa.eu/agriculture/sites/agriculture/files/statistics/facts-figures/farm-structures.pdf (2013).

k https://ec.europa.eu/eurostat/statistics-explained/index.php/Agriculture_statistics_-_family_farming_in_the_EU (2017).

l Lowder et al. (2016).

m http://www.fao.org/3/Y1860E/y1860e07.htm (2001).

n Based on per capita daily energy supply http://www.fao.org/3/mw252en/mw252en.pdf divided by kcals needed for healthy living (2015).

o https://www.business-standard.com/article/news-ians/nearly-70-percent-of-indian-farms-are-very-small-census-shows-115120901080_1.html (2015).

p https://www.business-standard.com/article/economy-policy/indian-farm-size-shrank-further-by-6-in-5-years-to-2015-16-census-shows-118100101057_1.html (2016).

q Moyo (2016).

r van Ittersum et al. (2016).

There are various other subcategories of farming, such as Mediterranean (adapted to specific climatic conditions) and organic (sustainable agricultural production relying on ecological processes, biodiversity, and practices adapted to local conditions rather than intensive inputs).

The interfaces between crops and the natural environment (the peri-agricultural environment) differ between large commercial farming and subsistence farming. In commercial farming, the peri-agricultural environment is usually controlled, and the ratio of crop-producing land area to peri-agricultural land area is high. In contrast, in small subsistence farming, there is often a close intermixture of farmed land and natural environment. Thus there are differences in the potential impact that an agricultural crop would have on the flora and fauna in the natural environment.

Nowadays, a large number of plant species have been domesticated to varying degrees. Table 1.2 presents 20 of the major crops which are grown worldwide or are major exports from tropical countries.

Table 1.2

⁎ Sugar produced.

⁎⁎ Oil produced.

a Data from https://en.wikipedia.org/wiki/List_of_most_valuable_crops_and_livestock_products

b Data from Leff et al. (2004).

2: Abiotic and biotic constraints on crop production

Any factors that impact on crop production will affect the consumers of crop products both in the subsistence farming system (which produces its own food) and the commercial system (which feeds mainly urban populations).

There are four major types of constraints on crop food production: abiotic reflecting the physical conditions under which the crop is grown or stored; biotic resulting from interactions that the crop plant has with other biological organisms; local socioeconomic and crop management factors; and genetic limitations on breeding for improvement of crop varieties. The first two types are discussed in this Section, the third in Section 3, and the fourth in Chapter 2, Section 2. An increasing number of these constraints have the potential to be addressed by molecular techniques which may require risk assessment (Chapter 2, Section 3).

Table 1.3 presents estimates of yield losses due to these factors for six food crops in sub-Saharan African and Asian smallholder farming systems.

Table 1.3

a Regions EAP, East Asia Pacific; SA, South Asia; SEA, South East Asia; SSA, sub-Saharan Africa.

b Averaged for different farming systems.

Data adapted from Waddington et al. (2010).

Most crop plants grow in environments that are suboptimal, which prevents them from attaining their full genetic potential for growth and reproduction (Bray et al., 2000; Rockstrom and Falkenmark, 2000). For example, US wheat yields in a record year can be up to eight times the average yield (Boyer, 1982), the difference being largely explained by abiotic stress factors which have been suggested to reduce average yields by 30%–50% worldwide for most major crop plants (Wang et al., 2003). In addition, plants must defend themselves against a wide range of biotic stresses. Each stress elicits a complex cellular and molecular response system from the plant in order to prevent damage and ensure survival, but often to the detriment of growth and yield (Herms and Mattson, 1992).

2.1: Abiotic constraints

Abiotic stresses are essentially unavoidable. Plants are especially, if not solely, dependent on environmental factors due to weather/climate conditions and the soil in which they are growing, so stresses due to these factors are particularly limiting.

2.1.1: Weather-induced constraints

The major weather-induced abiotic constraints on crop plants are the stresses induced by temperature (high and low temperatures), precipitation (excessive leading to flooding and lack of leading to drought), and salinity. Some estimates of global losses in crop yield due to these constraints are presented in Table 1.4.

Table 1.4

Heat and drought data are the averaged global crop yield losses due to the stress; Salinity data are the soil conductivity value (ds/m) that causes 50% loss in yield [soil conductivity of 4 ds/m (equivalent to 40 mM NaCl) is regarded as saline].

a Losses for each degree Celsius increase in global temperature. Data from Zhao et al. (2017).

b Data from Kim et al. (2019).

c Data from Panta et al. (2014).

The loss estimates in Table 1.4 are global, but regional and local losses are much higher where the actual event occurs, and these stresses can lead to local losses of up to 100%. The duration of weather events and combinations of weather events can cause increased losses. For example, excessive rainfall leads to maize yield losses similar to those caused by extreme drought (Li et al., 2019). Losses are exacerbated by combinations of stresses; cyclical water stress (drought or waterlogging) significantly reduced wheat yields when compared with single events (Ding et al., 2018). The extent of losses also depends on the crop growth stage at which the weather event(s) occur.

Weather is the condition of the atmosphere at a particular place over a short period of time, which impacts on the production of a specific crop at that time. Climate refers to the weather pattern, based on statistical data, of a place over a long enough period to yield meaningful averages. Different regions can have different climates. Thus overall change in climate leads to year-on-year weather changes.

These weather-induced factors are likely to be amplified by climate change, in which increases in atmospheric CO2 are linked to increases in atmospheric temperature which are in turn closely interlinked with changes in precipitation and extreme weather events (Appendix B).

2.1.1.1: Temperature

Temperature is a key factor affecting the rate of plant development, with each crop species having a defined range of maximum and minimum temperatures over which growth is observable (Hatfield and Prueger, 2015). Temperature affects the rate of growth, development, pollen production, and senescence of plants, and each crop species has a specific temperature range for the start of growth (base), pollen fertilization (optimum), and failure to produce grain or seeds (Table 1.5).

Table 1.5

Data modified from Hatfield et al. (2011).

Crop growth ceases below the base temperature and, below 0oC, crop plants are often killed by frost damage, though some crops (e.g., some Brassicas) can survive short periods of frost.

Exposure of plants to temperatures significantly higher than the optimum usually leads to heat stress which can have profound physiological effects, some of which have major impacts on crop yield. Plant reproduction is the most sensitive process in the plant lifecycle, and heat stress on cereal plants results in a reduction of tillers, fewer pollen grains, pollen sterility, and reduced pollen germination, which gives a lower yield (Hatfield and Prueger, 2015). It should be recognized that quoted values for effects on plant development and physiology are usually mean air temperatures; temperatures within the plant itself can be very different depending on factors such as the exposure to direct sunshine and the water status of the plant. Crop species have different lengths of anthesis (pollen release), maize having a very compressed period (a week or less), rice and sorghum having a medium period (a week or longer), and soybean and peanut having a long (several weeks) period. Even variations of temperature throughout the day can have effects on the viability of pollen. For example, maize pollen viability decreases rapidly at air temperatures over 35°C (Hatfield et al., 2011) and so, under heatwave conditions, varieties in which anthesis (pollen release) occurs early in the day would yield better than those in which anthesis is in the middle of the day.

Temperature will also affect the postanthesis period with elevated temperatures shortening the time for grain filling thus reducing the yield; temperatures above 25–30°C during grain-filling period significantly reduced wheat and sorghum yields (Chowdhury and Wardlaw, 1978).

Plants have defense mechanisms which may mitigate some of the heat stress effects on pollen (termed acclimation or thermo-tolerance) (Rieu et al., 2017; Jegadseesan et al., 2018), but relatively large increases in temperature (e.g., raised night temperatures or heatwaves) overcome this defense (termed collapse).

2.1.1.2: Flooding

The term flooding is often used to describe different situations in which the water excess can range from water-saturated soil (i.e., waterlogging) to deep water causing partial or even complete submergence of plants (Striker, 2012). Waterlogging affects just the roots, whereas submergence affects some, or all, of the upper parts of the plant depending on the developmental stage and the plant growth habit.

There are two forms of flooding: flash flooding which generally lasts for less than a week and deep water flooding which can last for several months. The effects of flooding are dependent on the plant species, the duration of flooding, and the temperature during flooding. However, most major crop species suffer severe water stress by flooding, especially by deep water flooding, but rice is highly tolerant of excess water stress (reviewed by Nishiuchi et al., 2012).

The main effects of flooding on plants are reviewed by Striker (2012). Shortly after the soil becomes waterlogged, the respiration of roots and microorganisms depletes the remaining oxygen and the environment becomes hypoxic (i.e., oxygen levels limit mitochondrial respiration) and later anoxic (i.e., respiration is completely inhibited). Thus the first constraint for plant growth under flooding is the immediate lack of oxygen necessary to sustain aerobic respiration of submerged tissues. As waterlogging time increases, there is a progressive decrease in the soil reduction-oxidation potential (redox potential) leading to the appearance of toxic compounds such as sulfides, soluble iron (Fe) and manganese (Mn), ethanol, lactic acid, acetaldehyde, and acetic and formic acids. Waterlogging affects many vital physiological functions of the plants such as photosynthesis, stomatal closure, and leads to growth inhibition of leaves, stem, and roots. It induces alteration of various plant metabolites that are related to important cellular processes such as energy and carbohydrate metabolism, amino acid metabolism, and phytohormone biosynthesis, all of which lead to a reduction in crop growth and yield. Complete submergence gives the most stressful scenario as both shoot and root plant compartments are underwater, and the chances to capture atmospheric oxygen and to continue with carbon fixation are restricted. Flooding duration is a major factor in determining plant survival following oxygen deprivation.

2.1.1.3: Drought

Agricultural drought is caused by precipitation deficiency coupled with high temperatures, strong winds, low relative humidity, more sunshine, and less cloud cover than normal for that region. These conditions result in soil water deficiency.

Crops differ in both the degree and stage of development in their sensitivity to water shortage (Brouwer et al., 1989) (Table 1.6).

Table 1.6

Data adapted from Brouwer et al. (1989).

In general, crops grown for their fresh leaves or fruits are more sensitive to water shortages than those grown for their dry seeds or fruits. As can be seen from Table 1.6, crops such as paddy rice, banana, potato, and sugarcane are very sensitive to water shortages which means that, if they are subjected to even slight water shortages, their yields will be reduced significantly. On the other hand, crops such as millet and sorghum have low sensitivity to drought, and the effect on yield will be slight if the water shortage does not last too long.

Brouwer et al. (1989) identified four stages in the growing season of an annual crop: the initial stage from sowing to about 10% ground cover, the crop development stage from about 10% to 70% ground cover, the mid-season stage including flowering and grain setting or yield formation, and the late-season stage including ripening and final yield. For almost all crops, the initial stage of germination and plant establishment is very sensitive to drought stress effects on survival. Once most crops are established, the mid-season stage is the most sensitive to drought stress effects on yield.

Plants perceive and respond rapidly to alterations in water status by a series of physiological, cellular, and molecular events developing in parallel (Chaves et al., 2009), with photosynthesis playing a central role in plant performance under drought conditions (reviewed by Pinheiro and Chaves, 2011).

2.1.1.4: Salinity

Detrimental salt concentrations in soil water (salinity) causing salt stress of crops affects nearly 20% of the world’s cultivated area and about half of the world’s irrigated lands, and is predicted to increase with climate change (Millennium Ecosystem Assessment, 2005; Koyro et al., 2008, 2014). Among the causes are drought, evaporation by high temperatures, irrigation, and intrusion of seawater in coastal areas exacerbated by rising sea levels due to melting of ice caps.

Salt stress adversely affects the productivity of crop plants (Negrão et al., 2017) by reducing plant cell membrane integrity, decreasing the activity of various enzymes, and impairing the function of the photosynthetic apparatus. Plants adapt to salinity by accumulating low molecular weight osmolytes such as proline and polyamines.

High levels of salinity cause heavy metal ion toxicity and decrease in nutrient uptake, creating osmotic imbalance and metabolic disorders that lead to disturbances in various physiological activities and decrease overall plant growth (Negrão et al., 2017). To cope with these adverse effects, some noncrop plants respond by changing gene expression, hormonal balance, and metabolite pools at the cellular level. When a plant is exposed to a stress condition, it reduces energy utilization for growth and development and shifts toward adjustment under harsh