The large and rapidly growing human population and climatic changes are challenges for world food security. For human food security, a significant increase in crop production is needed to avoid humanitarian crises in the future. In modern history, significant increases in crop production have been achieved via agrochemicals, classical breeding and genetically modified crops. However, based on progress achieved by these methods, further significant increases in crop production will require both current and novel multi disciplinary approaches. Microbial symbionts have great potential to help increase crop production to meet future demand. Microbial symbionts in crop production are a safe and sustainable technology that will be heavily incorporated in future agricultural systems. This review highlights briefly the role of various methods used to improve crop productivity and the possible role of microorganisms in agriculture.

Keywords: microbial symbionts, agrochemicals, breeding, genetically modified crops, sustainable agriculture

NSF, national science foundation; IAA, indole-3-acetic acid

Although progress in hunger reduction has been made at the global level the ultimate challenge to be conquered is food insecurity. Increases in the quality and quantity of food produced will be required to meet the increased demands of a growing population.¹ Global trends suggest that hunger reduction still masks disparities in food security that exist within and among populations. Globally as of 2009, 1.02billion people suffer from chronic hunger and one in seven people have an insufficient food supply to live an active, healthy life.² Continuing population and consumption growth will further increase the global demand for food. By 2050, the world population is expected to increase by 2.3billion to reach a total of 9.1billion and further exacerbate the international challenge of food insecurity.² Such population growth will necessitate the daunting task of increasing overall food production by 70–100%.^3‒5 If such a food production target proves to be unattainable, human populations in some areas of the world will face unavoidable starvation. Starvation is a humanitarian crisis with far-reaching effects. Hungry individuals are more likely to have clinical levels of anxiety and aggression, resulting in an angry population.⁶ Ongoing global climate change resulting in flooding, drought and heat waves will also significantly increase the difficulty of reaching the goal of nearly doubling crop production. At the same time food producers are experiencing increased competition for land, water, energy and other resources devoted solely to agriculture.^7,8

During the Green Revolution, farmers relied heavily on various agrochemicals (currently a $180billion market) to protect crops against plant pathogens and to increase production on nutrient-depleted soils. These practices showed remarkable success in increasing crop production worldwide and helped evade famine in many countries, while only requiring a 9-12% increase in crop area.⁹ Unfortunately, this Green Revolution based partially on agrochemicals was not sustainable and will not adequately address future food production needs. In addition, agrochemicals are expensive and can negatively influence the environment.^10‒13 For example agrochemicals have leaked into and polluted water sources and destroyed beneficial insects and microorganisms that are naturally present, making crops more susceptible to disease. Overall, the use of agrochemicals is still valuable under certain conditions and will no doubt continue. However, we must find safer and more sustainable alternatives to prevent and control agricultural pests and improve soil viability. For hundreds of year’s conventional plant breeding has allowed for the development of new varieties of crops via various selection methods, pure line hybrid technology and mutation breeding. Breeding programs have also contributed to the production of quality crops with higher nutritional values.¹⁴ Conventional breeding has increased corn yield for decades.¹⁵ However yield improvement gains due to breeding have leveled off or decreased in recent years for most staple crops,^16,17 demonstrating that conventional plant breeding alone will no longer sustain future global demand.

Engineering crops continues to improve yields and other important crop traits. Genetic modification of crops has increased herbicide tolerance, improved resistance to insects and environmental stress and generated valuable traits such as nutrient-enhanced seeds (such as Golden Rice with vitamin A).^18‒20 However these methods are relatively slow, expensive and applicable only to the most important crop species. Moreover, in many countries grower access to genetically modified crops is restricted because of bioethical and political concerns.²¹ Fifteen years after the introduction of the first genetically modified crops in the US, many farmers continue to raise concerns regarding the economic and environmental impacts, the evolution of resistant weeds and consumer acceptance of genetically modified crops.²² Additionally progress in the development of cultivars that can efficiently tolerate drought and heat waves while maintaining yield stability has been extremely slow. To date, Monsanto has developed the only commercial drought-tolerant maize (DroughtGard) through bacterial gene transfer. According to Monsanto, DroughtGard has an average yield advantage of 5 bushels per acre over competitor products when tested by 250 growers across the western Great Plains. Areport from Union of Concerned Scientists²³ claims that Drought Gard reduces crop losses only during moderate droughts and contends that it does not differ from other corn varieties interms of water use efficiency. However genetic engineering has significantly increased the quantity and quality of some crops; therefore, it has been proven beneficial for use in attaining the needed 70–100% increase in crop production. Following the predominant use of agrochemicals and conventional breeding during the Green Revolution andbillions of dollars spent on biotechnological approaches, the results show only a slight increase followed by a plateau in crop production.²⁴ The path to sustainable agriculture will not be based solely on the current, proven effectiveness of agrochemicals, breeding and genetically modified crops, but rather on devising new sustainable approaches to add to the improvements made possible by these methods, in hopes of reaching the targeted production increase. A sustainable agricultural system will require an interdisciplinary approach that integrates current and new technologies. Additionally, the new approach should not only focus on improving crop yields and mitigating the effects of climate change but must also consider other important ecological factors.

The application of symbiotic microorganisms in sustainable agriculture has immense potential for increasing crop yields and mitigating climate change with minimal disturbance to the environment.^25‒27 Microbial preparations will not only reduce the use of agrochemicals and improve the performance of crop varieties developed via breeding and genetic modification, but will also help in cycling nutrients and building soil structure. The use of a microbial symbiont with the reintroduction of multiple cropping systems has the potential to preserve and restore the natural microorganism populations present in agricultural lands. The use of symbiotic microorganisms is a novel approach that can inspire a new “Bio-Boom” similar to the Green Revolution of the past century. Endophytic bacteria and fungi are ubiquitous and ancient symbionts of almost all plant species, dating back over 400million years,^28,29 with a large influence on plant physiology. Their existence within plant tissues increases nutrient uptake efficiency, protects host plants against diseases as well as herbivorous and abiotic stresses and promotes the growth of foliage and deeper root systems.^30‒32 In the past the vast majority of plant productivity and physiology research has focused on plants as individuals. However plants constitute an ecosystem that harbors many other microorganisms including endophytic symbionts. Fortunately, many researchers are now focusing on the various microbiomes associated with wild and crop plants. High-throughput DNA sequencing, metagenomics, transcriptomics, proteomics and metabolomics approaches offer significant advancements in knowledge gained from examining plant microbiomes and their potential roles in sustainable plant productivity.^33,34 For example in-depth 454 sequencing has been used to reveal fungal endophyte communities in bur oak, mangrove and beech treestands,^35‒37 and metabolomic analyses have identified the roles that endophytic secondary metabolites play in their host plants.^38,39

Researchers are working on the discovery of new bacterial and fungal symbionts that improve crop productivity and other traits and are trying to understand the molecular mechanisms that govern the symbiotic relationship between plants and their symbionts. Many researchers have reported the discovery of microbial symbionts from wild and crop plants. Several of these symbionts show positive effects on crop productivity and stress tolerance of tomato, wheat, rice, barley, and other crops mainly under green house conditions.^40‒43 Microbial symbionts can increase plant productivity and stress tolerance via various mechanisms. For example, bacterial symbionts also known as plant growth-promoting rhizobacteria, can enhance plant growth via a variety of mechanisms such as improved nutrient solubilization and uptake,⁴⁴ nitrogen fixation,^45,46 production of volatile organic compounds⁴⁷ and modification of plant hormonal status.^48,49 Fungal symbionts can also improve plant productivity by various mechanisms including increased plant water-use efficiency maximized photosynthetic rate or increased production of metabolites such as the sugar trehalose or growth hormones such as gibberellins and auxin indole-3-acetic acid (IAA).^{31,43,50‒53} In addition fungal symbionts can regulate a diverse set of plant genes. For example Arabidopsis thaliana colonized by Piriformospora indica showed faster and greater up-regulation of nine drought stress-related genes⁵⁴ and in Theobroma cacao colonized with Trichoderma hamatum the endophyte altered expression of 19 drought-responsive genes and promoted greater seedling growth when plants were exposed to drought.⁵⁵ Over the last few years, public and private sector researchers have been racing to discover new beneficial soil microbes to improve crop production. Companies historically interested in breeding and biotechnology approaches are now investing in microbial products to promote sustainable microbial agricultural systems. Many other smaller agriculture-based companies have produced and sold microbial-based products that improve various aspects of crop production. In 2012 more than $ 2billion in agricultural microbe products were sold worldwide and sales are expected to grow by roughly 15% each year.⁵⁶ However this is a small fraction of agricultural expenditures compared to the $ 180 and $ 15.6billion spent on agrochemicals and biotechnology crops respectively.⁵⁷

The use of microbial symbiontsto increase crop productivity and stress tolerance is an essential step towards the new green revolution, the Bio-Boom. The Bio-Boom will significantly contribute to the development of friendly and sustainable agricultural systems that benefit both small and large farm producers due to their relatively low costs. In addition, the Bio-Boom will help bridge the gap between food production and the ever-growing human population. However one should note that the effectiveness of microbial symbionts vary by crop and habitat. Also careful consideration should be taken before introducing foreign symbionts into a new habitat. The use of habitat-specific microbial symbionts is key for a safe and successful Bio-Boom.

This publication was made possible by the National Science Foundation (NSF-1354050) and the U.S. Department of Agriculture’s Agricultural Marketing Service award number 14-SCBGP-AL-0001.

Author declares that there is no conflict of interest.

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