Gains and Losses of Agricultural Food Production:
Implications for the Twenty-First CenturyThis section is compiled by Frank M. Painter, D.C.
Send all comments or additions to: Frankp@chiro.org
FROM: Annu Rev Food Sci Technol 2022 (Mar 25): 13: 239–261 ~ FULL TEXT
OPEN ACCESS Slavko Komarnytsky • Sophia Retchin • Chi In Vong • Mary Ann Lila
Plants for Human Health Institute,
North Carolina State University,
Kannapolis, North Carolina
The world food supply depends on a diminishing list of plant crops and animal livestock to not only feed the ever-growing human population but also improve its nutritional state and lower the disease burden. Over the past century or so, technological advances in agricultural and food processing have helped reduce hunger and poverty but have not adequately addressed sustainability targets. This has led to an erosion of agricultural biodiversity and balanced diets and contributed to climate change and rising rates of chronic metabolic diseases. Modern food supply chains have progressively lost dietary fiber, complex carbohydrates, micronutrients, and several classes of phytochemicals with high bioactivity and nutritional relevance.
This review introduces the concept of agricultural food systems losses and focuses on improved sources of agricultural diversity, proteins with enhanced resilience, and novel monitoring, processing, and distribution technologies that are poised to improve food security, reduce food loss and waste, and improve health profiles in the near future.
Keywords: agricultural food systems; alternative proteins; biofortification; genetic improvement; phytochemicals; sustainable agriculture.
From the Full-Text Article:
INTRODUCTION
The earliest fossil evidence of modern humans (Homo sapiens) is 196,000 years old (Trinkaus 2005). The subsequent 150,000 years of uneven geographical expansion in eastern Africa and southeast Asia, and interactions with late archaic humans in western Eurasia, established the first cultural traditions in diets, technology, and ornamentation to produce significant shifts in our environments as early as 45,000 BCE (Vanhaeren & d’Errico 2006).
Increased competition for space and resources, at a time when most foods were directly acquired by hunting and gathering from the wild, led to rapid and often irreversible changes in the local environments. Larger populations led to the depletion of limitedly available wild food resources, diminishing the variety and range of accessible diets, thus limiting the theoretical global population of hunter-gatherers to a maximum of 10 million (Tallavaara et al. 2018).
Figure 1 As greater human densities eventually demanded more food than the local environments could provide, a gradual transition to cultivating crops and raising animals for food was initiated as early as 13,000 BCE (Diamond 2002) (Figure 1). This change, often referred to as the First Agricultural (Neolithic) Revolution, was neither intuitive nor obligatory, as no model cultivation practices existed prior to this point, and no clear foreseen consequences could be established to consciously initiate this transition. Traditional hunter-gatherer societies exhibited a range of hierarchical networks within nuclear families, foraging groups, and local tribes that ensured wide ecological and cultural diversity (Hamilton et al. 2007).
Hunter-gatherers cooked (Carmody & Wrangham 2009), stored, and transported ((Hammond et al. 2015) foods similarly to the subsequent societies, although their components changed substantially based on location and climate (Cordain et al. 2005). The average life spans of humans approached the 40s in the Upper Paleolithic and the 70s in the modern small-scale societies such as the Hadza people of Tanzania (Pontzer et al. 2018).
Finally, a recent metaanalysis of a typical hunter-gatherer diet indicated a macronutrient profile of 53% plants, 26% animals, and 21% fish (Crittenden & Schnorr 2017), with a slightly lower mean energy density (1.4–1.5 kcal/g) than that of modern industrialized populations (1.8–1.9 kcal/g) (Pontzer et al. 2018). Early hunter-gatherers also endured lower rates of infections (London & Hruschka 2014) and metabolic diseases (Raichlen et al. 2017) as a direct effect of the moderate to vigorous physical activity associated with their mobile lifestyle. Scarce remnants of collector hunter-gatherer societies such as the Ainu (Japan), who focused on exploitation of a single particular resource (fish), may represent an intermediate step between the mobile hunter-gatherers and the first sedentary societies.
We must consider, however, seasonal and temporal shifts in the human macronutrient intakes as the driving forces behind the transition to cultivation and domestication of food sources. Disease burden was a major limiting factor to early societies in highly productive (tropical) areas, whereas biodiversity was critical for less productive northern and southern environments (Loreau & de Mazancourt 2013). It is therefore very likely that the expanding hunter-gatherer societies found overcoming the low environmental productivity of temperate climates by means of gradual technological advances in cultivation and domestication easier than combating diseases of the tropical climates (Burger & Fristoe 2018).
Indeed, effective agricultural practices were introduced thousands of years before effective vaccines (Plotkin 2014) and antibiotics (Mohr 2016) were developed to address the spread of infectious diseases and associated epidemics. A review of the literature reveals six key gains in agricultural food production that supported these changes and allowed global food production to outstrip population growth:domestication,
farming practices,
food processing,
industrialization,
selective breeding, and
urbanization .Yet the race to provide a sufficient number of calories from supply-driven to demand-driven foods also resulted in increased environmental impacts and critical, often overlooked, losses to diversity, quality, and nutrient profiles that are discussed in more detail below.
AGRICULTURAL DOMESTICATION
Recent analysis of dental calculus and stone tools of the Neanderthal and early modern humans across the vast ranges of Europe, Near East, and Africa suggested that both populations gathered and consumed a variety of wild plants (Henry et al. 2014), with a particular focus on storage tubers, grass and legume seeds, and tree nuts (Shipley & Kindscher 2016). The same held true for aromatic plants like chamomile and yarrow that could have been used for culinary or medicinal purposes (Hardy et al. 2012). The duplication of starch-digesting genes (Larbey et al. 2019) and presence of functional bitter taste TAS2R (type 2 taste receptor) receptor variants (Lalueza-Fox et al. 2009) in these populations enabled multiple taster haplotypes and distinct responses to diverse plant phytochemical and carbohydrate loads (Palatini et al. 2016).
It is only logical to conclude that subsequent domestication of wild plants (and animals) for food consumption likely occurred in the geographical centers of abundance of each particular food resource, and these gains concurrently instigated the first measurable losses to our diets via losses in biodiversity (crop package), complex carbohydrates (lower glycemic index), micronutrients, and dietary fiber.
Loss of Crop Biodiversity (Crop Package)
Vavilov defined seven geographical centers of domestication (Ethiopia, Fertile Crescent, Mediterranean, China, South Asia, Mexico, and the Andes), and three more were subsequently added (Amazon, New Guinea, and eastern North America) (Smith 2006, Vavilov 1992). The revolutionary impact of emerging food production in these regions by cultivating plants and herding animals was further responsible for local population increases, driven by excess food and increases in numbers of children critical to farming and herding activities. The first Neolithic farming communities rapidly became essentially self-sufficient by establishing the narrow crop and animal packages that ensured their sedentary survival (Zeder 2008). The archaeobotanical data from eastern Mediterranean Neolithic sites identified a crop package of eight cultivated plant species, emmer (Triticum dicoccon Schrank ex Schubl), einkorn (Triticum monococcum L.), hulled barley (Hordeum vulgare L.), flax (Linum usitatissimum L.), lentils (Lens culinaris Medik.), peas (Pisum sativum L.), bitter vetch [Vicia ervilia (L.) Willd.], and chickpeas (Cicer arietinum L.) (Colledge et al. 2004), and four domesticated animal species, goats (Capra hircus L.), sheep (Ovis aries L.), cattle (Bos taurus L.), and pigs (Sus scrofa L.) (Zeder 2009).
Adoption of these agricultural packages led to rapid and major declines in the biodiversity of crops and animals in the settlements along the coast of the Mediterranean Basin (Colledge et al. 2004) as well as aromatic and presumably medicinal plants along the Danube-Rhine axis (Wagner et al. 2020). Multiple genetic studies have subsequently ruled out independent local ancestry of agricultural plants and animals, confirming the Near East as the primary source of the farming package (Weiss & Zohary 2011). Notable exceptions are a European domestic pig that replaced the original maternal ancestry of the Near Eastern swine (Larson et al. 2005) and wild rye (Secale cereale L.) and oat (Avena sativa L.) crops from independent European ancestry (Weiss et al. 2006). Isotopic data derived from a series of human remains also supports this conclusion, as they indicated a heavy early reliance on the diversity of species exploited for food and an abrupt shift toward a nearly exclusive domesticated terrestrial diet as farming economies were established (Tresset & Vigne 2007).
Losses in crop and varietal biodiversity became even more evident once trade routes and ever longer supply chains were established and expanded. Although many agricultural crops were introduced outside of their primary regions of diversity, the interconnected global food system increasingly relied on a narrow group of major energy-dense crops, including wheat, maize, and soybean, along with meat and dairy products, to fulfill calorie requirements (Khoury et al. 2014). This trend has driven a gradual increase in per capita calorie consumption in both the industrial and developing worlds (a shift from 2,410 to 2,950 kcal per person per day worldwide during 1970–2015), fueled by two- to fourfold increases in consumption of meats, sugars, and oils at the expense of pulses and roots/tubers (Kearney 2010). As a result, agricultural areas and relative proportions of crops are dominated by cereal and oils (>70%), with only three crops, wheat, maize, and rice, exceeding more than 10% of the crop markets (Leff et al. 2004). Relying on a global diet of such a limited diversity requires decoupling the geography of crop consumption from their production (Fader et al. 2013) and results in trade dependency for global food availability (Porkka et al. 2013).
The diminishing diversity of local crops and wild edible plants collected for consumption generally decreases the health and functionality of agricultural food systems at an unprecedented rate and magnitude. Uniform agricultural production systems are less resilient to changes in climate and pathogen patterns (Cabell & Oelofse 2012), whereas increasing cropping system diversity balances productivity, profitability, and environmental health (Davis et al. 2012). To compensate for and possibly rebuild the lost biodiversity in our food production systems, we need to understand the distribution and evolution of plant and animal indigenous pools (Dinssa et al. 2016), improve the available global geospatial records, and collect, organize, and preserve the diverse patterns of landrace populations and their wild genetic relatives. We also need to better understand the often substantial but variable contribution of crop biodiversity to the long-term stability of agroecosystems and its direct effects on other functional outcomes such as pollination, pest and disease control, soil nutrient dynamics, and carbon sequestration (Hajjar et al. 2008).
Loss of Dietary Fiber
The nutritional composition and content of our agricultural food production are also declining. Our ancestral feeding patterns included a mixture of vegetable foods (roots/tubers, fruits, beans, and nuts) naturally high in dietary fibers (Gaulin & Koner 1977). The primitive character of food processing preserved most fiber for direct human consumption, unlike the modern agricultural food systems that selectively reduce or eliminate dietary fiber during food processing (Schnabel et al. 2019). Dietary fiber has been recognized as resistant polysaccharides from plant cell walls (cellulose, lignin, hemicellulose) and noncellulosic components (pectin, gums, mucilage) that are unavailable for digestion (Dai & Chau 2017). Adequate intake of fiber is associated with a reduced risk of gastrointestinal, metabolic, and cardiovascular disorders (Mobley et al. 2014). Pulses (beans, peas, chickpeas, and lentils) contain 7–10 g dietary fiber in a standard half-cup portion, yet these crops make up only 22% of the 18 major crops produced in our agricultural food systems (Leff et al. 2004). An average pear or apple contributes 4–5 g of fiber to our diet, whereas the daily adequate intake of dietary fiber was identified in the range of 25–40 g (Clemens et al. 2012). Whole barley, oats, and rye have the potential to add 10–17 g of dietary fiber in a standard one cup edible portion, yet those are secondary cereal crops that are generally absent from the mainstream diets and popular low-carbohydrate dietary interventions (Quagliani & Felt-Gunderson 2016). Plant roots and tubers in their original or roasted forms (Wadley et al. 2020) historically provided a significant amount of carbohydrates and dietary fibers to the diets of primates (Hernandez-Aguilar et al. 2008) and early humans, yet modern agricultural systems are generally devoid of tubers and rhizomes, with the exception of the modern cultivars of potato, cassava, and sweet potato, which are relatively low in fiber (2–3 g). Developing a better understanding of the variety of insoluble (cellulose), insoluble but fermentable (hemicellulose), soluble but less fermentable (psyllium), or functional soluble fermentable fibers like ?-glucans (oats) or inulin (chicory) and incorporating these fibers into individual crop breeding programs and food processing strategies are critical requirements for the manufacture of a new generation of foods relevant to human health. Different types of fibers have different functional properties in the food matrix, especially as it pertains to shelf life, palatability, and support of the microbiome communities in the gut (Myhrstad et al. 2020). For example, the seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania was supported by an average daily consumption of 100–150 g of dietary fiber in the form of tubers, berries, and fruits (Smits et al. 2017).
Loss of a Wild Carbohydrates Profile
With the exception of soybean, all the top 10 most important agricultural crops are grown and consumed for their starch content (Campbell et al. 2016). The continuous decrease in dietary fiber content observed in modern agricultural foods also coincided with the abundance of digestible carbohydrates with a caloric availability that exceeds our metabolic requirements (Neel 1962). Human dietary specialization to increased carbohydrate loads was evident from recent genetic adaptations for the digestion of excess milk sugars (LCT, lactase) and plant storage carbohydrates (AMY1, salivary amylase) (Luca et al. 2010). Morphological and genetic modification of complex carbohydrate profiles is one of the key domestication traits introduced into our agricultural food systems in the past 10,000 years, and several gene clusters with large phenotypic effects account for most of the differences between the domesticated varieties and their wild ancestors. The major domesticated traits critical for crop cultivation were loss of seed dispersal (shattering), seed dormancy, and changes in plant stature (height and heading date); all of them are at least partially related to starch production and accumulation as major integrators in the regulation of plant growth (Sulpice et al. 2009). These early cultivation-related traits have been extensively researched and reported for wheat (Peng et al. 2003), corn (White & Doebley 1998), rice (Lee et al. 2005), soybean (Liu et al. 2007), tomato (Doganlar et al. 2002), and yam (Akakpo et al. 2017), among others. The findings indicated that genetic variation associated with plant biomass production determines the timing and speed of using plant metabolites to support growth and crop yields. Strongly represented are central carbohydrate metabolism-derived compounds such as glucose-6-phosphate, fructose-6-phosphate, succinate, citrate, and sucrose (Meyer et al. 2007).
Once in cultivation, crops were further selected for increased yield and carbohydrate content. Selection of new varieties ensured increased calorie retention at the expense of seed protein and mineral content (Harlan et al. 1973). Sweet corn was radically altered by selective breeding to accumulate four times as much sugar as its wild teosinte ancestor found in Mesoamerica, in part due to fixation of the homozygous recessive sugary1 allele in its genome that promotes sugar accumulation (Szymanek et al. 2015). In a typical corn plant, 75% of endosperm starch is present in the form of branched, insoluble amylopectin, and the remaining starch is stored as a linear amylose (Myers et al. 2000). Mutations in the waxy1 allele have been used in modern breeding to eliminate amylose and create high amylopectin plants (Tsai 1974), and starch branching amylose extender1 and debranching sugary1 alleles were selectively targeted during the domestication process (Whitt et al. 2002). In several crops, including wheat, corn, and yam, selective domestications led to the preservation of sus alleles, leading to starch formation by converting sucrose to fructose (Baroja-Fernández et al. 2012). It is also possible that the original domestication of corn was driven by the sugary content of its leaf and stalk tissues, similar to sugarcane and sugar beets, which accumulate sucrose (Smalley & Blake 2003).
Sweet watermelon stores 15% more water and three times as much sugar as its wild relative from Southern Africa (Ren et al. 2018). Sweet peaches increased edible flesh by 30% and water content by 20% compared to the wild relative, and although their fruit sugar content did not change dramatically, the overall net sugar intake has also increased (Vimolmangkang et al. 2016). A semidomesticated Tehuacan cactus [Stenocereus tellatus (Pfeiff.) Riccob.] bears colorful sweet fruits in marked contrast to the sour-tasting fruits of the wild populations (Casas et al. 1999). Many other crop plants evolved sugar-rich fruits to aid with seed dispersion by mammalian herbivory, and shifts toward higher sugar concentrations in storage organs under human cultivation were also noted in pepper, tomato, avocado, apple, mango, banana, and cherries (Spengler 2020). These changes were much less profound in vegetatively propagated root crops (tubers) and perennial fruit crops, which can be partially explained by fewer sexual generations following the initial domestication event (Clement 1999).
The most abundant free sugars in plants that are responsible for their sweet and pleasant taste are sucrose and maltose (disaccharides) and glucose and fructose (monosaccharides), and different agricultural crops accumulate different sugars in their tissues. Sucrose is a major transported sugar, in the range of 10–90 mmol/kg, in all crop cereals, whereas glucose is the most abundant free sugar in tubers (Halford et al. 2011). Increased incorporation of sugars into everyday diets in the form of high sugar-containing fruits, vegetables, and grains or as major components of processed foods leads to extreme spikes in blood sugar levels and promotes development of insulin resistance, diabetes, and obesity (Nusca et al. 2018). Active selection for naturally increased sugar content and the resulting sweetness (sucrose > glucose) of the newly developed crop food systems thus allows for the use of “natural” or “all natural” labels in the downstream food processing, which are generally preferred and often actively sought by the end consumers (Leyser 2014, Liu et al. 2017).
Loss of Micronutrients
Although fruits and green vegetables do not make a significant contribution to modern macronutrient intake, they are critical to the micronutrient status of the human body (Doughty 1979). Adoption of agricultural packages and the rise of processed foods significantly reduced, and in some instances completely eliminated, organ meats from modern diets. Currently, human diets rely on relatively micronutrient-poor muscle tissue to support the trace element status of the modern human body, especially in terms of B vitamins and minerals such as iron and zinc (Williams 2007). Because most vitamins and minerals present in whole animal and plant foods exist as biological complexes consisting of coenzymes and trace element activators, direct elemental supplementation is not always beneficial due to the inability to efficiently absorb, store, and metabolize these elements, especially among rapidly developing infants and children (Tako 2019). In some instances, fortification of the food supply with stable synthetic forms of micronutrients resulted in masking of other element deficiencies, as was shown for the folic acid–B12 interaction (Naderi & House 2018). As such, poor dietary diversity and low adequacy of micronutrient intakes not targeted by the national wheat flour fortification programs are still common in rural and developing regions (Rahmannia et al. 2019). Micronutrient deficiency in modern agricultural crops, driven by either scarcity or depletion of agricultural soils, decreased soil-to-crop micronutrient transmission, and the resulting scarcity in food and livestock feeds (Bevis 2015) suggests that realistic food-based approaches may not ensure dietary adequacy for young children and women (Ferguson et al. 2019).
Partial progress has been made to control micronutrient deficiencies through diversification of dietary crops, direct supplementation, biofortification of staple foods, and mycorrhizal-assisted and genetic modifications; however, many of these approaches fell short of the expected targets in their current form (White & Broadley 2009). Global adoption of modern varieties, agronomic practices, and/or historical breeding of edible crops to primarily improve yields and shelf storage coincided with dramatic declines in mean micronutrient concentrations in the dry matter of horticultural produce that cannot be efficiently reversed, as shown for semi-dwarf high-yielding wheat cultivars (Fan et al. 2008). Staple crop biofortification through gene stacking, using a rational combination of conventional breeding and metabolic engineering strategies (Van Der Straeten et al. 2020) or mycorrhizal microbial associations (Ye et al. 2020) may enable a new path forward to counteract these effects; however, the bioavailability of nutrients from many of these biofortified crops needs to be demonstrated globally. Finally, the targeted introgression of wild relative alleles can result in more than 50% higher grain protein and micronutrients, as was shown recently for barley (Wiegmann et al. 2019), or 3–10 times higher micronutrient levels through engineered expression of the target enzymes without directly affecting growth rates and storage-root yields of transgenic cassava (Narayanan et al. 2019).
CHANGES IN AGRICULTURAL PRACTICE
The industrial model that dominates modern agriculture relies on a large scale, reduced diversity, and increased chemical inputs to address soil depletion and pest and disease control. A dramatic increase in the rate of growth of agricultural productivity after 1950 improved food security, promoted economic growth, and generated large and long-lasting benefits in the form of globally decreased poverty and malnutrition. Diffusion of novel and more effective agricultural practices led to a threefold increase in cereal crop production with only a 30% increase in cultivated land (John & Babu 2021) and 2–5% reduction in infant mortality, with stronger effects among rural and poor households (von der Goltz et al. 2020). Crop genetic improvement focused predominantly on high-yielding, faster-maturing varieties (Eshed & Lippman 2019). However, most monoculture cropping systems and simplified large-scale landscapes were managed as crop factories rather than crop production ecosystems, thus exposing growers to greater risks and environmental uncertainties. Sudden losses of crops or livestock combined with the increased zoonotic pressure due to the factory-style management of agricultural resources have a high potential to accelerate host–pathogen dynamics, increase food prices, and amplify food insecurity in the near future.
Reduced Small-Patch Farming
Smallholder crop and livestock farming are on the decline globally, and this process appears to be largely irreversible because it is closely linked to a broader pattern of social transformation (Marini et al. 2011). These effects are especially significant in low-income countries that still have agricultural systems with low productivity, yet traditional farming households generally experience higher dietary diversity and less hunger even though a higher percentage of these households are poorer (Chakona & Shackleton 2017). Cropland aggregation into larger monoculture fields and smaller field margins generally leads to reduced diversity of arable crops and significant declines in seminatural and noncrop habitats and is directly responsible for the loss of the farmland biodiversity and associated ecosystem services (Clough et al. 2020). Recent data from landscapes with smaller fields showed 1.4–1.7-fold higher abundance in natural pollination and pest control (Martin et al. 2019). These issues can be addressed in part by incorporating new and diverse crop varieties, trees, and native perennials; reintegrating crops and livestock; reducing dependence on fertilizers and pesticides; and/or implementing farm practices specifically designed to mitigate evolving climate change, thus holding the key to making agriculture sustainable.
Production of Crops Outside of Native Habitats
All humans share a common ancestor that may have originated in East Africa; however, it is likely that natural selection and ecological resilience are largely responsible for the subsequent population differences in the ability to absorb, metabolize, and therefore tolerate different foods such as animal fat (Inuit people of Alaska), carbohydrates (Tohono O’Odham Indians of Arizona), dairy products (cattle herders of Southern Sudan but not the Ibo and Yoruba people of Nigeria), and alcohol (Pacific Islanders). Evolutionary adaptations to dietary changes driven by advances in food production systems can be found in multiple genetic loci that preserve historical signals of genetic shifts to different dietary regimes (Luca et al. 2010). However, both pharmacogenomic and nutrigenomic data in support of the link between certain gene variants and how the individual responds to the particular diet are equivocal and need to be further elucidated. A recent study that explored connections between 38 common nutrigenomic gene targets in a population of 500,000 individuals showed no significant relationship to health outcomes (Pavlidis et al. 2015), including weight loss (Gardner et al. 2018). Yet most of our staple foods are grown and manufactured in areas different from their origin, and the diversity of global food supplies continues to decrease (Khoury et al. 2014). Although expanding trade networks and global exchange of food commodities represent major advances in agricultural system development, it is counterintuitive to conclude that this expansion supports crop diversity around the world. Instead, many of the top crops consumed in each region of the world, as well as most of the food commodities traded on a large scale, are the same (Kummu et al. 2020).
Increased dependency on food imports directly correlates with increased homogeneity of world diets at the expense of regional staple foods that traditionally supplied a bulk of diversified nutrients to local populations. As such, the regional food landscapes lose their resilience when facing increased numbers of food shocks associated with conflicts and extreme weather events (Cottrell et al. 2019). Under the hypothetical event of complete synchronized failure in production within major commodities such as wheat, corn, rice, and soybean, the simultaneous global food losses are expected to peak at ?17% to ?34% (Mehrabi & Ramankutty 2019). Our best response to this challenge is to produce and provide a balance of nutrient-dense foods by simultaneously developing novel combinations of global market-based solutions to enhance nutrient density of major staple crops and support diverse regional production strategies that reflect food landscape, farmer, consumer, and climate priorities.
Loss of Genetic Diversity
Cultivating a limited number of crops not only reduced their own genetic diversity but also impaired the genetic diversity of other regional edible plants and their wild relatives. Regional crops evolved from their wild relatives through a long history of interactions with the environment, diseases and pests, and local human populations. Large amounts of the genetic diversity already collected by these societies in the form of heirloom varieties and landraces originating from multiple domestication and adaptation events represent one of the most important natural resources to ensure resilience and sustainability of future agricultural food systems (Weise et al. 2020). The genetic base of these collections can be further extended by incorporating crop wild relatives that possess many desirable traits (Castañeda-Álvarez et al. 2016). Once these genetic resources are efficiently preserved and monitored, there is also a critical need to establish continuous utilitarian value by making resources available for outside use, as has been established in, e.g., the Czech Republic (Taylor et al. 2017) and China (Kell et al. 2015). An often-overlooked resource for additional collections of regional breeds is the indigenous seed banks, as highlighted in 2020 by the Cherokee Nation becoming the first Indigenous nation in the United States to deposit its traditional seeds in the Svalbard vault. Feral populations of historically cultivated crops represent another untapped pool of genetic diversity. For example, feral rapeseed populations in Japan form distinct genetic clusters, many of which are closely related to rapeseed accessions in the NARO Genebank but some have unknown origins (Chen et al. 2020). Feral populations of Brassica oleracea found along Atlantic coasts in western Europe retain a wide range of self-incompatibility alleles that could be used to enhance the potential of breeding strategies designed to maintain heterosis (Mittell et al. 2020). In many cases when polyploidy preceded the domestication of the target crop, increased genetic diversity could be also derived from paleologs (Qi et al. 2021).
The process of genetic domestication and subsequent loss can be illustrated by cultivated varieties of cole vegetables (Brassica oleracea L.) that originated along the Atlantic shores and turnips (Brassica rapa L.) from the Hindu Kush mountains in Afghanistan (McAlvay et al. 2021). The release of their reference genomes allowed scientists to investigate the genetic diversity and evolutionary relationships that supported their specialized development of edible organs (Cheng et al. 2016). Nearly 95% of the Brassica landraces were subsequently lost within the past 100 years (Fowler & Mooney 1990, but see Heald & Chapman 2009). Similar genetic erosion was observed in tomato when the diverse bottlenecks experienced during domestication eliminated 95% of the genetic pool found in wild species (Fullana-Pericàs et al. 2019), generally in the direction of production traits at the expense of fruit quality and nutrition (Powell et al. 2012). However, when modern breeding efforts are gradually shifted to new traits sought by consumers (improved food quality and human health outcomes), the loss of genetic variation can be partially reversed (Schouten et al. 2019).
Globally, a high genetic erosion of crops is estimated at the rate of 1.5–2% per annum, with the highest rates recorded in 1920–1950s (13.2% per annum) and a continuous loss of 0.5–4% per annum in 1950–80s, as recorded in Italy (Hammer & Laghetti 2005). The loss of genetic variability represents both natural environmental selection due to climatic changes (Mercer & Perales 2010) and cultivation of high-performing F1 hybrids with a narrow genetic base (Muscolo et al. 2017). Commercial weight (yield), susceptibility to disease (Missio et al. 2018), and poor postharvest shelf life are the major factors that prevent incorporation of genetically diverse cultivars into modern agricultural production systems despite the increasing consumer demand for traditional and healthy foods. Nevertheless, because of their regional and historical success, these landraces are expected to harbor distinct genetic traits for nutrient uptake, utilization, and adaptation to stressful environments that can be effectively utilized in future crop breeding initiatives (Dwivedi et al. 2016).
ADVANCES IN FOOD PROCESSING
Ongoing economic and agricultural development trends, including increasing industrial food processing, nutrient preservation and fortification, urbanization, refrigerated transport, facilitated trade agreements and policies (subsidies), consumer purchasing power, supermarkets, convenience foods, and foods consumed away from home, resulted in a worldwide shift toward increased homogeneity of food choices. However, malnutrition in the form of both undernutrition and overnutrition is widespread and represents the single most important risk factor for the healthcare sector (Willett et al. 2019). The diversity and quality of food produced and consumed are decisive factors when evaluating future agricultural food systems for sustainability and public health outcomes, and increasing production and consumption of nutrient-dense foods is an obvious pathway to enhancing health and nutrition security.
Loss of Phytochemicals and Health Relevance
Diversity in food production and consumption is a key to improved nutrition and food security, and the current trend to improve sensory, health, process, and convenience qualities of food is driven primarily by consumers. These changes in consumer behavior highlight the health-promoting qualities of foods that were overlooked in favor of yield, disease resistance, and shelf-life traits because health-associated traits are invisible (in the sense that they are not directly associated with sensory experience in most cases) and take a long time to develop into the obvious physiological outcomes. As such, many of the health-associated macronutrients, micronutrients, and phytochemicals were unconsciously eliminated from the biochemical profiles of the domesticated crops. Although early humans relied on mixed diets of leafy greens, storage tubers, fruits (seeds, nuts), and opportunistic meats, diets based on modern crops show significant decreases in most health-promoting nutrients (tenfold for vitamin C, sixfold vitamin E, threefold for iron and zinc, twofold for folate and carotenoids) (Benzie 2003) and strong declines in many secondary plant metabolites that have predominantly defensive properties such as tannins, terpenes, and phenolic acids (Parr & Bolwell 2000). Although changes in macronutrients, micronutrients, and fiber associated with advanced food manufacturing systems are summarized in other parts of the study, this section focuses on phytochemicals (using polyphenols as an example) that may affect health but are not classified as essential nutrients.
Because of the biological activity of plant secondary metabolites and the putative human health outcomes associated with their intake, there is increasing interest in exploring wild relatives of agricultural crops, their heirloom and/or landrace varieties, and agricultural waste by-products that contain higher levels of phytochemicals than found in modern staple foods. One of the most prominent examples of these metabolites is phenolic compounds. Early hominids similar to their primate relatives critically depended on several hundred fig (Ficus L.) species native throughout the world and fed on their fruits and leaves (Milton 1999). Several isolated landraces of Ficus carica L. figs were reported to contain three- to eightfold higher amounts of phenolics (Hssaini et al. 2020) compared to their commercially cultivated varieties (Vallejo et al. 2012). Similarly, wild potato genotypes produced threefold increases in anthocyanins and soluble phenolics over the commercial cultivars (Wegener et al. 2009). The total phenolic concentrations observed in fruits of Andean tomato landraces were also higher than in commercial tomatoes (Asprelli et al. 2017), as the absolute variation in the metabolite abundance across the population tends to be much greater for secondary metabolites and may reach 100-fold values (Alseekh et al. 2015). Among 33 health-related phytochemicals belonging to four major groups of flavonoids and phenolic acids across 128 blueberry accessions of diploid, tetraploid, and hexaploid origin, the broad-sense heritability of the traits was moderate to high (H2 > 40%), suggesting that strong genetic factors control these traits (Mengist et al. 2020). The inherent diversity of phenolic metabolites, different levels of biological activity associated with hydroxylated and methylated metabolites (Skates et al. 2018), and substantial gastrointestinal metabolism of phenolics by resident microbiota (Kay et al. 2017) prevent us from defining a single strategy to select for a particular phenolic metabolite at this point, and more in-depth research on structure–activity relationships among different groups of phenolic metabolites is critically lacking. However, several successful attempts have been made to introgress phenolic traits from wild species to domesticated crops, including Sun Black tomato with enhanced anthocyanin production in the subepidermal tissue (Blando et al. 2019). Large variation has also been found for phenolic acid content among many cultivated species, which can be exploited to select varieties with higher phenolic content or identify parental materials for breeding programs (Kaushik et al. 2015).
Many phenolic compounds also contribute to taste perception by inducing bitter and/or astringent sensations in the oral cavity, which can be desired in certain foods like wines and ciders but is often rejected by the consumer in juices and other conventional foods. For this reason, bitter principles were mostly eliminated from food staples not only through selective breeding for sweeter (more appealing) traits but also by using a variety of debittering processes during food processing and manufacturing (Drewnowski & Gomez-Carneros 2000). Consistent with the knowledge that many plant-based foods have bitter tastes, higher-quality diets are intrinsically more bitter, and finding ways to increase acceptance of bitter tastes may increase diet quality at a population level (Cox et al. 2018). A new line of evidence emerged in the past five years that suggests that polyphenols inhibit glucose absorption in the gastrointestinal tract (Palatini et al. 2016) by interacting with the extraoral bitter receptors (TAS2Rs) (Palatini et al. 2017). Polyphenols interact with multiple TAS2Rs in the complex combinatorial pattern (Soares et al. 2018), and the effects of bitter principles on reducing glucose uptake and lowering postprandial blood glucose have been confirmed in several animal and clinical studies, including intragastric administration of quinine in a form of a mixed-nutrient drink (Bitarafan et al. 2020). These findings suggest that activation of extraoral TAS2Rs by dietary bitters contributes to promoting healthy nutrient–gut interactions that influence glycemia, gastrointestinal motility, and appetite; therefore, the disappearing bitter principles in modern diets may contribute to dysregulation of carbohydrate metabolism and development of metabolic disorders. Additionally, complexation of polyphenols with plant proteins can be designed as ingredients to stabilize food structures, modulate bitter polyphenol flavors, and increase delivery of health-protective polyphenols and proteins in the diet (Diaz et al. 2020). Cases like this close the gap between perceived and inherent quality of foods and substantiate the selected breeding of old and new crops, biofortification of food products through targeted plant nutrition, and optimized application of emerging technological solutions to develop a new definition of quality for agricultural food products (Kyriacou & Rouphael 2018).
Loss of Traditional Foods in Favor of Novel Foods
Not only are traditional crops less represented in food supply chains and genebank resources around the world but their decreasing consumption further depletes phytochemical and micronutrient profiles of the human diet already affected by lesser nutrient quality and content in modern staple crops (Ebert 2020). Traditional crops are generally not included in public and private sector investments and policies (Schreinemachers et al. 2018), but they hold a key to improving nutritional and health outcomes among the smallholder farmers and rural communities in developing countries (Timler et al. 2020). Community-based seed production of traditional crops supports the diversity of health foods, generates additional incomes, and improves the ecological resilience of local communities (Meldrum et al. 2018). Traditional subsistence eaters from three isolated Inuit communities in Nunavut consumed, on average, a more nutrient-dense diet and achieved better dietary adequacy than others consuming commodity foods (Sheehy et al. 2015), but ensuring a nutritionally adequate complementary feeding diet for infants based on traditional foods alone is difficult (Ferguson & Darmon 2007). An interesting example of replacing commercial maize with landrace blue maize varieties for the production of traditional masa and tortillas in the Southwest was described recently, albeit significant modifications to nixtamalization and other processing steps were required (Chimimba et al. 2019). Many traditional foods are leafy green vegetables that represent one of the most nutrient-dense groups of foods (Ghosh-Jerath et al. 2016), yet these types of food typically experience high postharvest losses, largely due to limited food processing, preservation, and storage capacity in developing countries (Kuyu & Bereka 2020). Therefore, promoting traditional foods for human and environmental health will remain a priority in future agricultural food systems, and additional nutrition research into the nutritive value of neglected crops is warranted because the health benefits of many of these foods have been largely unexplored.
Loss of Conventional Ripening
Major advances in food processing and preservation, including refrigerated transport and packaging, dramatically increase global food safety and availability (Sridhar et al. 2020). With modern breeding efforts to increase the yields, firmness, and shelf life of many agricultural crops, the long, arduous process of shipping and distributing these foods globally often relies on early-maturing varieties and/or under-ripe produce. Along with causing customer dissatisfaction due to taste and aroma changes associated with under-ripening, these foods are also known to contain lesser amounts of health-promoting phytochemicals, as shown for antioxidant nonfluorescing chlorophyll catabolytes in apples and pears (Müller et al. 2007), anti-inflammatory anthocyanins in berries (Siriwoharn et al. 2004), and anticancer non-provitamin A carotenoid lycopene in tomato (Powell et al. 2012). Another example is the shift from red coloration of many fruits being the sign of high fruit quality and optimal ripening stage to the selection of mutant lines that accumulate epidermal anthocyanins in low light conditions, thus protecting the expected financial return of under-ripe fruits at the expense of their organoleptic properties (Iglesias et al. 2008). Compromised phytochemical profiles and ripe fruit quality in exchange for desirable production traits will need to be addressed in future breeding efforts, especially if investments in fruit and vegetable value chains that focus on improved processing, storage, and distribution technologies could improve health profiles, reduce food losses and waste, and create new value-added products through development of novel extraction and drying technologies to transform and decrease food waste (Sagar et al. 2018).
EMERGING TRENDS AND TECHNOLOGIES
The modern foods we eat and agricultural systems that produce them have evolved rapidly with the recent changes and advancements in science and technology, and several new initiatives hold great promise in revolutionizing agricultural food production.
Alternative Proteins
Figure 2 To fulfill the projected 76% rise in meat demand by 2050 without extensive environmental degradation, the definition of meat is being reimagined (Godfray et al. 2018). The category of traditional animal-derived meats has expanded to include a diverse and rapidly evolving group of meat analogs that attempt to replicate the physical, nutritional, and gustatory properties of meat in a sustainable and ethical fashion. Five of the most advanced alternative protein technologies in either commercial or late research stages are plant protein (plant-based foods), new animal sources (insect), cultivated meat (animal cell culture), microbial protein (bacteria, fungi, or algae biomass fermentation), and recombinant protein (precision fermentation) (Figure 2). Plant-based protein is the most well established and is currently derived from dry or wet fractionated, protein-rich seeds. Soybeans, wheat, and peas are the main crops used for protein extracts, chosen mainly for their functional properties, which are essential for meat analog structure formation, such as oil holding capacities, solubility, emulsification, and gelation properties, as well as their nutritional value (Kyriakopoulou et al. 2019). Other crops such as chickpeas, peanuts, oats, lupine, algae, and fungi are being used in protein concentrates but are currently limited by cost, functionality, incomplete amino acids, and undesirable flavor profiles. The immediate critical need for these initiatives is to establish new breeding programs that focus specifically on the quality of legume seeds to select for higher protein levels and superior functionality for use in future plant-based meats (De Ron et al. 2017).
Plants are expected to be the largest source of alternative protein in the near future because of customer preferences and limited environmental footprint. To compare favorably with animal cell culture (regenerated animal cells from a limited number of animal donors, propagated in vitro to mimic animal tissues and the same protein profile) and mushroom protein (filamentous fungal biomass produced in fermentation), plant protein manufacturers have the option of balancing the incomplete amino acid profiles by incorporating complementing types of protein concentrates derived from different plant species (Bohrer 2019). Although soy isolates offer lower costs and digestibility-corrected amino acid scores comparable to that of meat, potential allergenic and health effects must be considered (Katz et al. 2014). Other plant proteins developed in this space must improve current processing technologies to produce a high-protein quality product with minimal color and taste (peas, among others). Finally, to mimic the texture of animal-derived meat, the majority of alternative proteins are currently extruded to generate fibrous-like structures (Zahari et al. 2020), a process that simultaneously improves protein digestibility but reduces its nutritional value and phytochemical profile (Martin et al. 2019). Alternative strategies such as shear cell technology and 3D printing may alleviate some of these concerns. There are also opportunities to formulate alternative proteins with complementary combinations of plant-based, animal cell, mycoprotein, and/or recombinant protein ingredients to create novel alternative animal products that maximize the different qualities of various ingredients, as has been suggested for leghemoglobin (Ismail et al. 2020).
Cellular Agriculture and Fermentation
Cellular agriculture defines a group of technologies that utilize cell cultures of various origins (animal, plant, algal, microbial, fungal) to produce agricultural commodities in bioreactors (Mattick 2018, Rischer et al. 2020), although the term is often used more narrowly to define manufacturing of animal cell culture–based products (cellular aggregates or acellular proteins and/or fats), as described in the previous section. Harvesting food products in agricultural settings places inherent limits on their use, functionality, safety, and environmental footprint, especially in animal agriculture where the conversion rate of feed to animal product is rather low at 15% (Post 2014). By reassembling agricultural foods and materials from their basic cell components obtained from the pathogen-free, axenic cultures, cellular agriculture attempts to reinvent food staples so they can be customized to specific qualities, functionalities, and culinary purposes, and multiple human health or well-being outcomes. Cultured meat consists of engineered tissue-specific cells, culture media, scaffolds, texturizers, flavors, and/or colorants that are reviewed elsewhere (Jairath et al. 2021). In its current form, cultured meat aims to become biologically equivalent to at least ground or minced meat products, as postmortem metabolism, texture, flavor, and nutritional composition of fresh meat are difficult to achieve (Fraeye et al. 2020). It is also not clear how the profiles of essential amino acids, fatty acids, vitamins, and micronutrients will be affected in the various final products (Thorrez & Vandenburgh 2019). The health effects of these products are expected to be inferior to plant-based meat analogs, which were recently shown to decrease several cardiometabolic risk factors, including trimethylamine-N-oxide, LDL cholesterol, and weight after consuming ?2 servings/day of plant- or animal-based protein for 8 weeks each (n = 36) (Crimarco et al. 2020).
Whole-cell microbial cultures that require additional processing steps to access nutrients accumulated within the host cells have long been used in various applications relative to agricultural food production and are reviewed elsewhere (Grimm & Wösten 2018). Direct biotechnological manufacturing and secretion of the acellular targets by native or engineered cells holds a high promise of delivering a variety of nutritional and flavoring components useful for incorporation into alternative animal products (Rischer et al. 2020). The concept of plant cells as foods or dietary ingredients offers an attractive alternative of healthy raw materials (Valdiani et al. 2019), as plant systems are well suited for continuous secretion and acellular accumulation of proteins (Komarnytsky et al. 2004) and other value-added products (Shi et al. 2021), including whole-cell formulations (Georgiev et al. 2018) and novel conceptual foods (Nordlund et al. 2018).
Controlled Environment Agriculture
Controlled environment farming is considered another important technology to advance agricultural food production. A modern combination that spans artificial intelligence–controlled environments, greenhouse space, vertical farming, and urban agriculture is projected to scale current agricultural crop production to a growing global population and promote local foods. Lowering the cost or improving the productivity of any controlled environment agriculture (CEA) automation solution is expected to directly benefit long-term food safety and sustainability while improving the quality, nutrition, and taste of the agricultural crops (Shamshiri et al. 2018). This approach has proven efficient for growing leafy greens and certain herbs, although a narrow range of crops, higher costs, and energy dependence remain the important limiting factors behind modern agricultural innovation systems (Pigford et al. 2018). The use of super dwarf plant varieties may allow extension of CEA to globally relevant food staples such as wheat (Asseng et al. 2020) and rice (Schmierer et al. 2021), although indoor single-layer greenhouse-based farms in which sunlight supplements the artificial lighting are more realistic at this point (Avgoustaki & Xydis 2020). The unequal access and distribution of future benefits to developing and marginalized populations will remain an inborn challenge of the described technological advances (Nally 2016), and the costs of these technologies will likely be prohibitive to the producers (Barnes et al. 2019). As such, the social and ethical impacts of this transformation remain to be elucidated (van der Burg et al. 2019).
CONCLUSIONS
Multiple developments in food production and processing, ever-expanding trade networks, and the global exchange of food commodities represent a series of major advances that have reduced hunger and poverty around the world. The ability to successfully continue this trend into the future to meet the world’s food needs rely in part on our capacity to address the following critical gaps in modern agricultural food systems:(a) the decreasing number of globally relevant food staples, reduced genetic diversity of main crops and their wild relatives, and loss of traditional foods;
(b) the declining nutritional value of modern diets in favor of energy-dense foods driven by the low adequacy of micronutrient, fiber, and phytochemical profiles of modern crops; and
(c) greater risks and environmental footprints of large-scale industrial agricultural practices that lead to decreasing diversity and quality of processed foods and generation of enormous food waste streams.Although the collateral losses of modern food manufacturing have been known for a long time, our ability to address these issues has changed dramatically with the recent advancements in science and technology, including our ability to understand and manipulate the distribution and evolution of plant and animal genetic resources, expansion of conventional breeding to include biofortification, mycorrhizal-assisted and genetic modifications, gene stacking, CRISPR-Cas genome editing, and artificial intelligence–CEA technologies to mitigate food supply, safety, climate, and health-related outcomes in making agriculture sustainable. In the future, it may be expected for the global market that a minimum quality of foods will be in part mandated and regulated based on the levels of their bioactive constituents with proven health outcomes.
DISCLOSURE STATEMENT
S.R. is a cofounder of the Chapel Hill Alternative Protein Project and held internships at MeaTech 3D and Peace of Meat. The authors are not aware of any other affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
This work was funded in part by the USDA National Institute of Food and Agriculture Hatch project 1023927 (S.K.).
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