Enhancing food security amid climate change through rewilding and de novo domestication

Abstract

Global food production is dominated by a few major crops such as maize, wheat and rice.Historically, the breeding of these crops has primarily focused on increasing yield potential and secondarily on enhancing biotic and abiotic resistance to help achieve and protect that potential. Although agricultural outputs have increased in modern times due to both genetic gain and improvements in agronomy, the current rates of yield improvement for most crops will almost certainly be insufficient to meet projected future food demands. Climate change is already having a negative impact on agriculture by creating local conditions which are suboptimal for current agricultural practice and germplasm. This will be exacerbated given future projections of global climate change. One study projected that maize yields could decline by 24% under a high greenhouse gas emission scenario due to increases in temperature and shifts in rainfall patterns, among other factors (Jägermeyr, 2021).Step changes in increases in local and global production, either from germplasm improvement or modified agronomic practice are required, but such major improvements have been implemented infrequently. A notable example of a step change towards increasing crop yields is the pioneering work of Norman Borlaug, credited with being the father of the first green revolution. As part of a whole system's approach, Borlaug introduced dwarfing genes into modern crops, preventing lodging tendencies and increasing the harvest index, thereby allowing much greater yields driven by higher inputs of nitrogen (Swaminathan 2009).However, boosting crop yields by adding large amounts of nitrogen and water, for example, is not a sustainable approach. In fact, inefficient use of nitrogen can have serious environmental consequences. Whilst it is an essential element to enhance plant development and growth, nitrogen fertilizer that is not taken up by crops but instead leaks into the ecosystem can lead to water pollution, the release of greenhouse gases, soil acidification, etc. (Govindasamy et al. 2023).Furthermore, high yielding cropping systems may be particularly susceptible to abiotic and biotic stresses as driven by changing climatic conditions, leading to variable harvests and hence compromised yield stability. Present and future food security will depend on improving current crops and cropping systems towards increased intrinsic yield potential and higher resistance to environmental stressors. This is particularly relevant when we need to raise production in naturally low yielding environments as common across the globe or to extend cropping areas where conditions are currently suboptimal. It requires embracing a wide variety of novel approaches to crop improvement, including but not limited to exploiting genetic diversity in breeding programs, exploitation of under-utilized crops, de novo domestication of resistant but low yielding germplasm, and potentially involving precision breeding technologies of gene transformation and genome editing.In recent years, many abiotic stresses associated with non-optimal temperature and precipitation patterns during the growing season have become more widespread and extreme due to climate change. Suggestions of a future positive 'fertilizer' effect of increasing atmospheric carbon dioxide levels on yield (Food and Agriculture Organization, 1996), will most likely be offset by changing influences of temperature and rain patterns, for example as shown for wheat (Zhao et al 2017), with both ambient and extreme events having negative impacts on crop metabolism, development, fertility and productivity. Furthermore, such abiotic stressors influence biotic interactions, often enhancing pathogen abundance, spread and efficacy. In addition, changing climatic conditions can have multiple impacts on soil health, including waterlogging or drying as well as affecting soil biodiversity. In many regions, extreme climate events, such as more frequent and intense droughts, severely limit productivity often due to restricted water availability. Lack of water can be overcome by irrigation systems, however, in many cases this process raises soil salt content leading to a new, anthropogenically created, soil salinity stress. Soil salinity has a major negative impact on crop production and regions affected by salinity stress, specifically due to irrigation activities, are increasing worldwide (Atta et al 2023). Whilst most major crops have minimal tolerance to saline environments, there are many salt-tolerant plants, but these are generally not cultivated as crops due to their limited economic value or lack of desirable agricultural traits.Consequently, yield potentials of most crops are seldom achieved in most areas of the globe, due to one or more biotic or abiotic environmental stresses, often made worse by climate change. This failure to achieve yield potential results in a 'yield gap', that is the difference between theoretical achievable yield with a defined germplasm compared to what is practically achieved by a farmer. This difference is often substantial, impacting on farmer incomes and food security. Furthermore, these yield gaps appear to be steadily increasing for many crops (Gerber et al 2024).Yield and productivity are extremely complex multigenic traits involving multiple physiological and developmental processes and are inevitably underpinned by a large number of genes. Interactions with abiotic stressors are likely to be just as complex. Furthermore, tolerance and resistance to most stressors are conferred by multiple mechanisms. Direct engineering of such traits via targeted gene manipulation is possible in exceptional circumstances, namely where only a limited number of genes are required to confer enhanced resistance. In such cases, it is feasible to introduce genes or alleles from ancestral resistant germplasm in a so-called 'rewilding' approach using targeted or precision breeding. In their lead article published in Frontiers in Science, Palmgren and Shabala (2024) discuss the rewilding approach by bringing genes lost from wild ancestors back to domesticated crops in order to increase salt tolerance or resistance.More commonly an approach of selection of improved varieties by conventional breeding is taken. However, conventional breeding, which can be slow and complex, will always be limited by the genetic variation and gene pool size that exists for a crop, although recent work in wheat suggests that only a fraction of available diversity in landraces is utilized in the modern breeding pool (Cheng et al 2024). Wider crossing with ancestral relatives may provide even further diversity, including greater tolerance to many unfavorable conditions (Baker et al 2020;King et al 2024). Nonetheless, even with increased diversity, resilience to environmental stressors within the gene pools of common crop species may be still rather limited.A radical alternative approach to adapting crop production to adverse cultivation conditions would be to diversify our present food sources and increase the use of some of the many under-utilized crops, whose current wide adoption is mainly limited by low yields. Such species should be chosen based on their natural resistance to extreme temperatures, limited water availability and increased salinity; environmental phenomena that are already affecting current agricultural output and are anticipated to become an even greater threat for future production. The main challenge would be to improve the yield potential of these plants.Whilst domestication of most major crops has taken many thousands of years, this process may be replicated in a targeted and accelerated approach utilizing our modern knowledge of the minimal genes required to produce cultivatable crops in a process termed de novo domestication (Østerberg et al 2017;Palmgren and Shabala, 2024). For this to be successful, identification of the key traits which enable acceptable yield to be obtained under cultivation is required. Such traits include harvest index, size of the harvested component (e.g. grain, fruit, fiber, etc.), characteristics of seeds to facilitate collection, for example seed harvestability through lack of shattering, and adaptation to local environments in terms of photoperiod and thermal temperature requirements throughout the growing season. Many of the genes or loci required for domestication are already well known in cultivated species and artificially engineering these domestication traits in the stress-resistant wild species, using genome editing or genetic manipulation, is within the reach of current technology. Farming will need to adapt to the cultivation of novel crops, requiring substantial financial investment, and therefore ensuring consumer acceptance will be paramount to economic viability.Food security is the most pressing challenge for society and will be solved primarily by agriculture. Historically, both plant breeding and optimized agronomic practice have resulted in steady incremental improvements in agricultural outputs, including greater resistance to abiotic and biotic stressors. However, meeting the ever-increasing demands for production whilst resisting the increasingly extreme impacts of various stressors -often enhanced by climate change, and also driven by the needs to farm in less optimal environments-will require new and novel technologies, including advanced plant breeding. Key amongst such technologies, as outlined by Palmgren and Shabala (2024), are re-wilding by reintroducing 'lost' traits and de novo domestication of wild species with inherent resistance.Author contribution