Phytomicrobiome Coordination Signals Hold Potential for Climate Change-Resilient Agriculture

Abstract

A plant growing under natural conditions is always associated with a substantial, diverse, and well-orchestrated community of microbes-the phytomicrobiome. The phytomicrobiome genome is larger and more fluid than that of the plant. The microbes of the phytomicrobiome assist the plant in nutrient uptake, pathogen control, stress management, and overall growth and development. At least some of this is facilitated by the production of signal compounds, both plant-to-microbe and microbe back to the plant. This is best characterized in the legume nitrogen fixing and mycorrhizal symbioses. More recently lipo-chitooligosaccharide (LCO) and thuricin 17, two microbe-to-plant signals, have been shown to regulate stress responses in a wide range of plant species. While thuricin 17 production is constitutive, LCO signals are only produced in response to a signal from the plant. We discuss how some signal compounds will only be discovered when root-associated microbes are exposed to appropriate plant-to-microbe signals (positive regulation), and this might only happen under specific conditions, such as abiotic stress, while others may only be produced in the absence of a particular plant-to-microbe signal molecule (negative regulation). Some phytomicrobiome members only elicit effects in a specific crop species (specialists), while other phytomicrobiome members elicit effects in a wide range of crop species (generalists). We propose that some specialists could exhibit generalist activity when exposed to signals from the correct plant species. The use of microbe-to-plant signals can enhance crop stress tolerance and could result in more climate change resilient agricultural systems.

Keywords: biostimulants; crop; phytomicrobiom; signal compounds; stress resiliance.

FIGURE 1

Examples of positive (left side) and negative (right side) regulation of microbe-to-plant signal production by plant-produced signals. Positive regulation (left): the plant root secretes a plant-to-microbe signal compound that activates microbe-to-plant signal compound production. Negative regulation (right): the plant constitutively produces a plant-to-microbe signal compound that inhibits production of a microbe-to-plant signal compound. When expression of the plant-to-microbe signal compound is downregulated, production of the microbe-to-plant signal compound occurs.

FIGURE 2

Examples of specialist (left side) and generalist (middle). Specialist (a): a specific signal (red arrow, e.g., LCOs) is only expressed in the presence of a specific plant-to-microbe signal compound (green arrow, e.g., isoflavonoids) produced by specific crop species A (e.g., a specific legume). Generalist (b): a general signal (purple arrow) is expressed in the presence of a general plant-to-microbe signal compound (blue arrow) produced by a wider range of plants, such as crop species B. In some cases, exogenous application (Specialist to Generalist c) of a specific signal (green arrow) could result in the production of a microbe-to-plant signal by a microbe that usually functions as a specialist—the microbe-to-plant signal can be recognized by a wide range of plant species and the microbe is converted from a specialist into a generalist one (e.g., if the plant-to-microbe signal from crop species A is applied to a microbe in the presence of crop species B). For example, exogenous application of a specific plant-to-microbe signal (e.g., genistein, an isoflavonoid from soybean, in a legume nitrogen-fixing symbiosis) results in the production of the microbe-to-plant signal (e.g., LCO) in the rhizosphere of a wide range of plants, where the microbe-to-plant signal has an alternative function (e.g., regulation of plant stress responses).