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11 July 2024

From ‘Farm to Fork’: Exploring the Potential of Nutrient-Rich and Stress-Resilient Emergent Crops for Sustainable and Healthy Food in the Mediterranean Region in the Face of Climate Change Challenges

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Agrarian Research Institute “La Orden-Valdesequera” of Extremadura (CICYTEX), 06187 Guadajira (Badajoz), Spain
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Technological Institute of Food and Agriculture of Extremadura (INTAEX-CICYTEX), Avda. Adolfo Suárez s/n, 06007 Badajoz, Spain
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Instituto de Biomedicina de Sevilla, IBiS/Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, 41013 Seville, Spain
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Departamento de Bioquímica Médica y Biología Molecular e Inmunología, Facultad de Medicina, Universidad de Sevilla, 41009 Seville, Spain
This article belongs to the Special Issue Effects of Environmental Factors on Nutritional Quality of Plant Seeds and Other Edible Plant Parts

Abstract

In the dynamic landscape of agriculture and food science, incorporating emergent crops appears as a pioneering solution for diversifying agriculture, unlocking possibilities for sustainable cultivation and nutritional bolstering food security, and creating economic prospects amid evolving environmental and market conditions with positive impacts on human health. This review explores the potential of utilizing emergent crops in Mediterranean environments under current climate scenarios, emphasizing the manifold benefits of agricultural and food system diversification and assessing the impact of environmental factors on their quality and consumer health. Through a deep exploration of the resilience, nutritional value, and health impacts of neglected and underutilized species (NUS) such as quinoa, amaranth, chia, moringa, buckwheat, millet, teff, hemp, or desert truffles, their capacity to thrive in the changing Mediterranean climate is highlighted, offering novel opportunities for agriculture and functional food development. By analysing how promoting agricultural diversification can enhance food system adaptability to evolving environmental conditions, fostering sustainability and resilience, we discuss recent findings that underscore the main benefits and limitations of these crops from agricultural, food science, and health perspectives, all crucial for responsible and sustainable adoption. Thus, by using a sustainable and holistic approach, this revision analyses how the integration of NUS crops into Mediterranean agrifood systems can enhance agriculture resilience and food quality addressing environmental, nutritional, biomedical, economic, and cultural dimensions, thereby mitigating the risks associated with monoculture practices and bolstering local economies and livelihoods under new climate scenarios.

1. Introduction

Considering the current trends in population growth, achieving global food security remains a future challenge in which agriculture plays a key role []. Currently, agriculture is based on the monoculture of a limited number of species []. This practice leads to increased fragility of the agricultural system (e.g., in the face of biotic and abiotic stresses), resulting in a depletion of available food ingredients, as our diet relies on a few plant species [,]. Furthermore, there is substantial scientific evidence indicating that more diverse agrifood systems are generally safer from both nutritional and agronomical perspectives, showing greater resilience to environmental changes and offering a broader array of nutritionally effective food products []. Indeed, growing a variety of crops enhances the nutritional diversity of the local diet. This is particularly important for certain communities that rely heavily on a few staple crops, helping address nutritional deficiencies and improve overall health [,]. Introducing novel crops will also offer farmers supplementary income streams, diminishing dependence on a singular crop and alleviating the financial risks associated with market fluctuations or adverse weather conditions []. Particularly, certain crops may be more resilient to drought, heat, or other climate-related challenges, providing a buffer against the impacts of climate change []. Also, diversifying crops into a rotation system helps break pest, weed infestation, and disease cycles, improves soil fertility, and reduces the risk of soil degradation [] supporting sustainable agricultural practices. Likewise, the diversification of our agricultural system can contribute to minimizing food dependence that may be subjected, as we have experienced in recent times, to changes linked to international conflicts [].
Currently, two-thirds of the plant-based foods we consume primarily come from three cereals, wheat, rice, and maize, providing 60% of dietary energy []. While the nutritional value of these crops is undeniable, they are deficient in essential nutrients crucial for ensuring a healthy and balanced diet, such as minerals, proteins, essential amino acids, or vitamins, among others [,]. Therefore, the diversification of our food crops (for human and animal consumption), by including crops with high nutritional value, is essential for achieving a balanced nutrient intake and promoting greater sustainability and moderation in the consumption of animal-origin foods [].
The distinct climatic patterns of the Mediterranean region are characterized by mild, wet winters and warm, dry summers []. The unique climatic conditions and diverse ecosystems of these areas face increasing challenges derived from climate change which are linked to the escalating occurrence of droughts and elevated temperatures, which directly impact agriculture []. Also, pests and diseases may proliferate under altered climate conditions, posing additional challenges for farmers []. Furthermore, rainfed agriculture, which plays a pivotal role in southern and eastern Mediterranean countries, makes a substantial contribution to food security in the region []. Therefore, the Mediterranean agrifood system will require the development of adaptation strategies to cope with the aforementioned climatic changing conditions, giving special consideration to rainfed agriculture, particularly in light of its importance in relation to its extent in terms of surface area. This may involve the cultivation of more resilient crop species, which include neglected and underutilized species (NUS) and improved (bred) crop varieties, changes in farming practices, and the implementation of sustainable agricultural techniques to mitigate the impact of climate change, among others [,].
NUS, a novel and evolving category in agriculture, holds profound significance for global food security, particularly in addressing nutritional challenges. These crops represent a diverse array of plant species that exhibit resilience and adaptability. Their emergence is a response to the pressing need for sustainable and nutritious food sources, mostly when considering the challenges faced by conventional crops, such as susceptibility to pests, diseases, and climate change, especially in susceptible regions such as the Mediterranean [,,]. They are promising alternatives for cultivation in diverse ecosystems and their adaptability can contribute to increased Mediterranean agricultural productivity [].
Overall, it should be considered that the widespread adoption of agricultural diversification practices in the Mediterranean region can contribute to establishing a more sustainable and effective agriculture and food system at both local and global scales []. The cultivation of new crops can boost rural economies by creating employment, supporting local businesses, and contributing to overall economic growth. However, it is important to note that the successful introduction of new crops requires careful consideration of factors such as soil suitability, climate conditions, market demand, and farmers’ capacity to adapt to new cultivation practices, among others []. Additionally, supportive policies, extension services, and research initiatives play a vital role in facilitating the successful integration of new crops [].
Taking all these aspects into consideration, this review aims to explore the potential of nutrient-rich and stress-resilient emergent crops as a viable solution to foster sustainable and healthy food production in the face of climatic challenges in the Mediterranean region. By examining the adaptability and nutritional value of selected NUSs (including quinoa (Chenopodium quinoa Willd.), amaranth (Amaranthus spp.), chia (Salvia hispanica L.), moringa (Moringa oleifera Lam.), buckwheat (Fagopyrum esculentum Moench and Fagopyrum tataricum (L.) Gaertn.), millet (including Panicum miliaceum L. or Setaria italica L., among others), teff (Eragrostis tef (Zucc.) Trotter), hemp (Cannabis sativa L.), or desert truffles (including Terfezia claveryi Chatin)), we aim to shed light on their role in mitigating the adverse effects of climate change on agricultural systems. This work not only delves into the agronomical features of these crops but also considers their nutritional, food technological, and health characteristics, emphasizing the importance of diversifying crops in the Mediterranean region for resilient and nutritionally rich food sources. Through this exploration, we aspire to contribute to the development of strategies that promote food security and sustainability in the Mediterranean region amidst the dynamic landscape of climate change.

4. The Health Benefits of NUSs for the Mediterranean Region

Globally, developed countries are experiencing an increase in the incidence of major non-communicable diseases such as cardiovascular disease, diabetes, and obesity. This increase has led to a significant rise in morbi-mortality and healthcare expenditure []. The search for novel foods that not only provide balanced nutrition but also have multiple beneficial health effects has made the study of functional foods an incipient field. In this context, the health-promoting aspects of bioactive compounds found in NUS, such as quinoa, chia, amaranth, hemp, moringa, sorghum, buckwheat, teff, or dessert truffles, have been elucidated. Quinoa and amaranth, in particular, not only have commendable nutritional profiles but are also significantly richer in both micro- and phytonutrients than conventional grains, which has led to a growing interest in these crops for potential integration into functional foods and nutraceuticals []. Recent studies have focused on quinoa and amaranth intending to identify numerous bioactive compounds, including phenolic acids, flavonoids, betalains, carotenoids, and tocopherols. These compounds have been found to have significant antioxidant, -inflammatory, -hypertensive, and -hyperglycaemic and lipid-lowering properties, and are the main mechanistic basis for their beneficial effects against cancer, neurodegeneration, and metabolic disorders such as obesity and diabetes, which are major risk factors for cardiovascular disease []. By and large, quinoa and amaranth are generally considered safe for consumption and are not commonly associated with allergies, although isolated cases have been reported []. However, more research is needed to fully understand the prevalence and mechanisms of amaranth and quinoa allergy.
Chia seeds also have excellent nutritional properties []. In addition to their high fibre content and balanced range of macro- and micro-nutrients, chia seeds are known for their high concentration of α-linolenic acid, which serves as a precursor for the synthesis of ω-3 fatty acids with long chains such as DHA and EPA. It is now well established that omega-3 polyunsaturated fatty acids (PUFAs) confer several health benefits. In particular, the consumption of omega-3 fatty acids has been associated with a decrease in triglyceride and non-high-density lipoprotein cholesterol levels, supporting the protective role of these fatty acids against cardiovascular events []. In addition to reducing dyslipidaemia, omega-3 fatty acids also exert protective benefits against atherosclerosis, inflammation, diabetes, and cancer, although some research findings are controversial and highlight the need for more clinical studies to clarify the beneficial effects of ω-3 PUFAs []. Chia seeds provide health benefits due to bioactive compounds such as phenolic molecules, tocopherols and carotenoids. These compounds have antioxidant properties that contribute to health benefits, particularly in the fight against diseases such as diabetes and cancer []. Chia seeds also contain phytosterols, which are mainly associated with reduced cholesterol and hepatoprotective effects. They also play a beneficial role in diabetes and cardiovascular diseases [].
In recent years, the distinctive components and biological activities of moringa have been extensively studied and documented, highlighting its potential health benefits and therapeutic applications []. The whole M. oleifera plant, including leaves, fruits, pods, flowers, seeds, and roots, exhibits a range of biological activities. Leaves are rich in active constituents such as flavonoids, polyphenols, terpenoids, phenylpropanoids, fatty acids, sterols, and alkanes, as well as vitamins and minerals [,,,]. Among these, flavonoids and polyphenols are the primary bioactive molecules, showing antioxidant, -cancer, -sepsis, -inflammatory, -hypertensive, and -diabetic and hepatic lipid-lowering properties and beneficial effects on obesity-related reproductive diseases. In addition to fatty acids, essential amino acids, and flavonoids, the seeds also contain isothiocyanates, which play an important role as anti-inflammatory, -oxidant, -bacterial, and -cancer agents []. Furthermore, newly discovered components extracted from the stem of the plant, such as tricosanoic acid, cholest-5-en-3-ol, stigmasterol, and gamma-sitosterol, have shown potent antifungal activity []. Potent antioxidants such as tocopherols, ascorbic acid, flavonoids, and carotenoids have also been extracted from M. oleifera flowers [].
Hemp seed, derived from the plant Cannabis sativa L., has a rich history of use in Asia dating back to prehistoric times. Recently, countries such as the United States, Canada, and Australia have now legalized the farming and use of hemp seed, provided that its tetrahydrocannabinol content remains below 0.3%. This legalization has increased interest in hempseed due to its recognized nutritional benefits and perceived pharmaceutical applications [,]. Historically, the economic importance of hemp has been in the use of the fibre-rich stem, valued to produce textiles, clothing, and paper goods, while its seeds have remained largely underutilized. However, in recent years there has been a surge of interest in exploring the nutritional and pharmaceutical properties of hemp. In particular, hempseed oil has the highest concentration of PUFAs of any vegetable oil. It is widely accepted that an increased intake of PUFAs is associated with a reduced risk of several health conditions, including cardiovascular disease, cancer, rheumatoid arthritis, hypertension, inflammatory disorders, and autoimmune diseases. Of note is the highly desirable ω-6:ω-3 ratio found in hempseed, which typically ranges from 2.5 to 3.5/1, in contrast to the ω-6:ω-3 ratio found in typical Western diets, which normally ranges from 15 to 17/1. The importance of the ω-6/ω-3 ratio in human health is well documented, with a high ratio (>10:1) in the human diet being associated with an increased risk of cancer, inflammation, and cardiovascular disease. On the contrary, a ratio lower than 2.5:1 has been associated with a reduced risk of chronic diseases, the suppression of cancer cells, and lower mortality []. In addition to its oil content, cannabis seeds contain two different phenolic compounds: lignanamides and hydroxycinnamic acids. In vitro studies have extensively documented the antioxidant properties of hempseed lignanamides, including compounds such as N-trans-caffeoyltyramine and cannabisin B. Additionally, hempseed is rich in flavonoids, which contribute significantly to its antioxidant capabilities, as demonstrated by cell-free system assays such as ORAC and FRAP. Furthermore, the different fractions obtained from hempseed processing show different levels of antioxidant activity, with the coarsest fraction, dominated by hulls, showing the highest potency in this regard []. Hemp seed also contains a higher concentration of tocopherols than most vegetables. These tocopherols have antioxidant properties that effectively inhibit the oxidation of unsaturated fatty acids []. Furthermore, the potential health benefits of cannabinoids, including CBD, have been explored in relation to various conditions such as Alzheimer’s disease, cancer, epilepsy, inflammatory diseases, Parkinson’s disease, and amyotrophic lateral sclerosis, as observed in studies conducted in mice []. In general, preclinical studies indicate the beneficial effects of hempseed supplementation on improving the blood lipid profiles and levels of linoleic acid, α-linolenic acid, and γ-linolenic acid. These enhancements have been associated with improvements in metabolic syndrome and neurodegenerative diseases []. In human trials, while several studies have described the beneficial effects of hempseed oil on skin health, mental well-being, and neurological disorders, the effects of hempseed on cardiovascular disease require further verification. Existing studies have produced conflicting results, indicating the need for further research (revised by []).
The health benefits of foods made from sorghum grain lie in the fact that sorghum is a rich source of antioxidant compounds such as vitamins, as well as macro- and micro-nutrients, including phenolic acids, flavonoids, and sterols []. The high antioxidant activity of bioactive compounds in sorghum grain is mainly due to its polyphenolic composition. In particular, white sorghum flour contains almost twice as many polyphenols as red sorghum flour. Numerous studies have demonstrated the anti-obesogenic effects of sorghum. Extracts of this grain have been shown to significantly inhibit the differentiation and accumulation of triglycerides. In addition, sorghum-supplied diets have been shown to reduce body weight in rats []. Human clinical trials have been conducted with sorghum to investigate obesity-related parameters. Participants who consumed sorghum biscuits reported greater satiety than those who consumed wheat-based products []. Additionally, sorghum starch undergoes slower digestion compared to starch from other cereals because of the hard outer layer of the endosperm and the existence of tannins. As a result, findings from these investigations indicate the possible incorporation of sorghum into diets for weight control.
Buckwheat is rich in several bioactive compounds that, along with essential nutrients, contribute to positive health outcomes []. More than a hundred bioactive compounds have been identified in buckwheat [], including high levels of flavonoids such as rutin (quercetin-3-d-rutinoside), epicatechin, and quercetin, which vary depending on the type and origin of the buckwheat [,,]. Moreover, the level of phenolic compounds is highly dependent on the roasting process, which can affect the total content and lead to significant losses []. Although the available literature indicates that buckwheat supplementation may provide some benefit in lowering TC and glucose in the context of dyslipidaemia and type 2 diabetes, a recent systematic review and meta-analysis have shown a small association between buckwheat supplementation intervention and cardiovascular risk factors []. Therefore, future human trials are needed to unveil the beneficial effects of the bioactive compounds in buckwheat.
Teff, another gluten-free pseudo-cereal like quinoa and buckwheat, has attracted considerable research interest due to its many potential health benefits. The use of teff is an opportunity to address the nutritional shortcomings of current commercial gluten-free products. Rich in insoluble polysaccharides, as well as macro- and micro-nutrients, teff is being explored as a viable option for people with type 2 diabetes due to its low glycaemic index. Teff is also naturally high in iron, making it suitable for people with anaemia []. Teff also contains higher levels of minerals such as zinc, iron, and calcium than other grains []. Furthermore, ferulic acid, a phenolic acid compound known for its potent antioxidant properties, is a major component of teff, along with other bioactives such as flavones like apigenin-6,8-c-diglucoside and apigenin-8-c-glucosyl-7-O-glucosides [].
Furthermore, many of these NUSs contain antinutritional compounds such as phytic acid and saponins, which have the potential to bind nutrients and reduce absorption in our bodies. However, the use of various processing techniques such as fermentation, sprouting, extrusion, and cooking can increase their bioavailability [].
Finally, it is important to emphasize the importance of bioactive peptides derived from the NUSs. These peptides, typically 2 to 50 amino acids in length, remain inert within the intact protein. However, when released by proteases during digestion or through external hydrolysis, they are absorbed by the intestinal tract, reach various organs, and modulate important biological activities. These activities include immunomodulatory, antioxidant, antihypertensive, hypolipidaemic, hypoglycaemic, and hypotensive effects. Such effects play a key role in metabolic diseases such as obesity, metabolic syndrome, or metabolic-associated fatty liver disease [,,,]

5. Future Prospects

In the context of global economic and climatic change, a deeper understanding of agricultural production intensification is required, and new opportunities and challenges must be identified to progress []. Following high-input resource-intensive farming systems, an innovative approach is needed to protect and enhance natural resources while increasing productivity. Emerging crops appear capable of ensuring future food security and sovereignty []. They contribute to climate change mitigation and adaptation, demonstrating resilience and adaptation to abiotic stress [,,,] For instance, salinization and drought are two major factors altering conditions for crop growth. Quinoa, a facultative halophyte, can withstand high salinity levels and water scarcity [], and amaranth enriches its nutritional content and antioxidant activity under stress conditions []. Furthermore, chia has proven to be a viable option in dry, sandy soil and high-temperature environments [], growing successfully in water-limiting situations [], as does desert truffle []. Additionally, these crops require lower inputs for productivity, resulting in the limited use of water, fertilizers, and pesticides [,,]. This makes NUSs pivotal in reducing greenhouse gas emissions [] and promoting the sustainable development and efficient management of natural resources such as water, soil, and air. Moreover, NUSs promote soil protection, aligning with the objectives of the EU policy (CAP 2023–27), aiming for a 20% reduction in fertilizer use by 2030 and the potential to preserve and improve soil health [].
NUSs also hold the potential for phytoremediation, offering a feasible option to mitigate the effects of heavy metal stress. Different species exhibit varying degrees of heavy metal accumulation and tolerance mechanisms. Using these species as a phytoremediation approach is seen as an optimal solution for reclaiming soil contaminated with heavy metals, ensuring the safety of harvested crops for human consumption. Quinoa, for instance, has shown promising bioremediation potential for soil contaminated with heavy metals [], while amaranth has been studied extensively for remediating cadmium (Cd)-contaminated agricultural soils [].
Therefore, meeting the needs of a growing world population by 2050 will require more resources from intensive food production. Monocultures may be vulnerable to unpredictable climate change, potentially leading to severe productivity losses. As previously mentioned, crop diversification, especially through the rotation of underutilized crops with existing systems, can improve food security, disrupt disease and pest cycles, replenish soil nutrients, and diversify pollinator presence []. Additionally, the increasing demand for ingredients used in animal feed creates pressure on major crops. In line with this, NUSs can serve as alternative sources of energy and protein, reducing dependence on major crops and competition with human food purposes. These crops could play a crucial role in animal growth and productivity due to their nutritional qualities. For example, Amaranth leaves and grains have shown varied nutritional qualities depending on consumption by monogastric or ruminants [,,]. Quinoa, with its protein-rich fodder, offers an opportunity to diversify its use beyond animal feed.
Thus, NUSs have the potential to play a crucial role in addressing the world’s current food challenges. They offer sustainability, adaptability, and nutritional value that can contribute to food security, conserve agrobiodiversity, and make agricultural and agrifood value chains more resilient. Despite limited progress in the development of superior underutilized crops, greater efforts will be needed to integrate these crops into mainstream agriculture.

6. Conclusions

In conclusion, the exploration of emergent crops in the dynamic context of agriculture and food science presents a groundbreaking avenue towards sustainable cultivation and nutritional innovation, with profound implications for human health. This review has delved into the potential of utilizing NUSs in Mediterranean environments, shedding light on the manifold benefits of diversifying agricultural and food systems. The resilient nature, nutritional richness, and positive health impacts of NUS such as quinoa, amaranth, chia, moringa, buckwheat, millet, teff, hemp, and desert truffles have been thoroughly examined, emphasizing their adaptability to the changing climate. By embracing these crops, we unlocked novel opportunities for agriculture and functional food development in important susceptible agricultural areas such as the Mediterranean region, paving the way for a more resilient and adaptable food system. The analysis made extends beyond the agronomic and nutritional aspects, delving into the broader dimensions of environmental, biomedical, economic, and cultural significance. Promoting agricultural diversification emerges as a key strategy to enhance food system adaptability to evolving environmental conditions, fostering sustainability and resilience. Therefore, by integrating these crops into our agrifood systems, we not only bolster agriculture resilience but also enhance food quality, addressing a spectrum of dimensions crucial for sustainable development. In essence, this revision calls for a paradigm shift towards embracing emergent crops, highlighting their potential to redefine our approach to agriculture, food science, and health. The integration of neglected and underutilized species into our food systems represents a forward-thinking solution, steering us towards a more sustainable and resilient future.

Author Contributions

All authors have contributed to writing—original draft preparation. All authors have read and agreed to the published version of the manuscript.

Funding

The authors gratefully acknowledge the financial support received from the Agencia Estatal de Investigación—Ministerio de Ciencia e Innovación (MICINN, Spain) (RED2022-134382-T).

Acknowledgments

This paper is dedicated to the memory of Maria del Carmen Blazquez Blazquez, for her support and inspiration. All listed authors in the authorship are on behalf of NutriCrop Spanish Consortium/Group integrated by María Reguera Blázquez (coordinator) (maria.reguera@uam.es); Isaac Maestro Gaitán (isaac.maestro@uam.es); Ingrid Aguiló Aguayo (ingrid.aguilo@irta.cat); Gemma Echeverria (gemma.echeverria@irta.cat); Maribel Abadias (isabel.abadias@irta.cat); Nieves Aparicio Gutiérrez (apagutni@itacyl.es); Ana Belen Martin Diana (mardiaan@itacyl.es); Daniel Rico Bargues (daniel.rico@uva.es); José Moisés Laparra Llopis (moises.laparra@imdea.org); Antonio Carrillo Vico (vico@us.es); Patricia J Lardone (plardone@us.es); Ignacio Bejarano Hernando (ibejarano@us.es); Eduardo Ponce España (eponce-ibis@us.es); Cristina Soler Rivas (cristina.soler@uam.es); Francisco R. Marín Martín (francisco.marin@uam.es); Joan Casals Missio(joan.casals-missio@upc.edu); Ana Rivera Pinzano (ana.rivera@upc.edu); Sònia Campo Sanchez (soniacampo@fundaciomiquelagusti.cat); Justo Javier Pedroche Jiménez (j.pedroche@csic.es); Claudia Mónika Haros (cmharos@iata.csic.es); Javier Matías Prieto (javier.matias@juntaex.es); María José Rodríguez Gómez (mariajose.rodriguezg@juntaex.es); Verónica Cruz Sobrado (veronica.cruz@juntaex.es); Patricia Calvo Magro (patricia.calvo@juntaex.es); Nieves Fernández García (nieves@cebas.csic.es); Enrique Olmos (eolmos@cebas.csic.es); Sara Fondevilla Aparicio (sfondevilla@ias.csic.es); Asunción Morte Gómez (amorte@um.es); Alfonso Navarro Ródenas (anr@um.es); José Eduardo Marqués Gálvez (joseeduardo.marques@um.es); Felicidad Ronda Balbás (mfronda@uva.es); and Pedro Antonio Caballero Calvo (pedroantonio.caballero@uva.es).

Conflicts of Interest

The authors declare no conflicts of interest.

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