Symbiotic Root-Endophytic Soil Microbes Improve Crop Productivity and Provide Environmental Benefits

Abstract

Plants should not be regarded as entities unto themselves, but as the visible part of plant-microbe complexes which are best understood as "holobiomes." Some microorganisms when given the opportunity to inhabit plant roots become root symbionts. Such root colonization by symbiotic microbes can raise crop yields by promoting the growth of both shoots and roots, by enhancing uptake, fixation, and/or more efficient use of nutrients, by improving plants' resistance to pests, diseases, and abiotic stresses that include drought, salt, and other environmental conditions, and by enhancing plants' capacity for photosynthesis. We refer plant-microbe associations with these capabilities that have been purposefully established as enhanced plant holobiomes (EPHs). Here, we consider four groups of phylogenetically distinct and distant symbiotic endophytes: (1) Rhizobiaceae bacteria; (2) plant-obligate arbuscular mycorrhizal fungi (AMF); (3) selected endophytic strains of fungi in the genus Trichoderma; and (4) fungi in the Sebicales order, specifically Piriformospora indica. Although these exhibit quite different "lifestyles" when inhabiting plants, all induce beneficial systemic changes in plants' gene expression that are surprisingly similar. For example, all induce gene expression that produces proteins which detoxify reactive oxygen species (ROS). ROS are increased by environmental stresses on plants or by overexcitation of photosynthetic pigments. Gene overexpression results in a cellular environment where ROS levels are controlled and made more compatible with plants' metabolic processes. EPHs also frequently exhibit increased rates of photosynthesis that contribute to greater plant growth and other capabilities. Soil organic matter (SOM) is augmented when plant root growth is increased and roots remain in the soil. The combination of enhanced photosynthesis, increasing sequestration of CO₂ from the air, and elevation of SOM removes C from the atmosphere and stores it in the soil. Reductions in global greenhouse gas levels can be accelerated by incentives for carbon farming and carbon cap-and-trade programs that reward such climate-friendly agriculture. The development and spread of EPHs as part of such initiatives has potential both to enhance farm productivity and incomes and to decelerate global warming.

Figure 1

Plant endophytic symbiotic microorganisms are able to enhance plant growth and development from seedlings to maturity, as evidenced by these examples from the use of Trichoderma with corn. (a) Ten-day-old seedlings of an inbred maize line (Mo17) grown from untreated seeds (upper row) or from seeds treated with T. afrohazianum (lower row). The differences in size that are seen in the seedlings persist in the mature plants. (b) Appearance of corn plants in a commercial trial in Minnesota. The plant on the right was grown from a seed treated with a commercial product containing T. afroharzianum and T. atroviride overtreated onto a standard chemical pesticide, while the plant on the left grew from a seed treated only with a chemical pesticide. Photo courtesy of Advanced Biological Marketing. (c) Both the organisms and their SAMPs can induce season-long changes that affect both shoots and roots. Shown are roots of mature corn plants grown from either seeds treated only with a chemical pesticide (left) or with similar seeds overtreated with the SAMP 1-octen-3-ol at picoliter quantities (right). The observed increase in root growth is distant both temporally (several months later) and spatially from the site of application of the SAMP. Photo courtesy of Advanced Biological Marketing. (d) Trichoderma strains increase rooting depth. Corn plants were grown in the field to maturity, and then, trenches were dug adjacent to them about 2.3 m deep. The soil faces next to the plants were treated with a power washer to expose root intercepts and were marked with map pins that show up as dots in the figure. At 25–75 cm below the soil surface, there were about twice as many roots from plants grown from Trichoderma-treated seeds as from untreated seeds [6].

Figure 2

Packing of Trichoderma viride biofertilizers in a village production center in Tamil Nadu state of India initiated by the M.S. Swaminathan Research Foundation in Chennai [109].

Figure 3

Diagrammatic presentation of how plants and their photosystems are protected from damage by ROS, which is induced by both stress and by photoexcitation. All of the endophytes described in this article have the ability to countervail ROS damage. We hypothesize that this result occurs in better-functioning plants that have optimized internal redox potential.

Figure 4

Summary of groups of endophytic microorganisms considered in this paper and summary of mechanisms and systems by which they enhance plant productivity.