Manipulation of plant ethylene balance by soil microbiota: a holobiont perspective to stress tolerance

Abstract

Plants continuously adjust their physiology and phenotype to stressors. Plant hormones and modulators mediate the adaptation of the plant to changing environmental conditions by allocating resources precisely between growth and stress tolerance. Plant responses to stressors are typically studied without considering the associated microbiota. However, plants live in association with a wide range of microbiota, which alter the whole plant life history. Here, we would like to place microbiota as an important determinant of plant mediate stress responses. Microbiota could filter stress for plants or alter the plant physiology and hormonal balance. Ethylene is one of the most important regulators for plant growth, development and response to stressors. Plant ethylene pathway is modulated by plants, but also by associated microbiota; microbiota could up or down regulate plant ethylene production by a wide range of bacterial traits, and potentially affect ethylene-mediated regulation of stress responses. Studies on plant physiology confirm the crucial role of ethylene in stress tolerance. However, in plant-microbe interactions, ethylene reduction by the action of ACC deaminase enzyme of microbiota is mainly considered as a trait that promotes plant growth, especially under stress conditions. Here, we study the ACC deaminase enzyme of bacteria in the context of recent advances of ethylene studies in plant physiology. We show that reduction of ethylene by bacteria decreases the cadmium uptake in plants, as ethylene is an important modulator of nutrient uptake. As large-scale soil decontamination is practically impossible, using microbiota as biotechnological tools to reduce heavy metals in soils may contribute to safer food and feed production. We further show that ethylene reduction by microbiota may alter plant stress tolerance. While ethylene reduction by ACC deaminase-producing microbiota might have some advantages for plants in non-stress conditions, it may also interfere with common plant responses to stressors such as heavy metal or submergence. Interestingly, this part of our results contrasts with the current paradigm in plant-microbe interactions which considers the ACC deaminase enzyme as a plant growth promoting trait under stress conditions. This part shows that ACC deaminase producing enzyme has predominantly negative effects on plant fitness under stress condition. We further show that ethylene reduction by microbiota depends greatly on bacterial genetic background, which means that ACC deaminase enzymes with different bacterial genetic background significantly alter the outcome of plant-microbe interaction effects.We finally conclude that ethylene signalling cannot be fully understood without considering the whole microbiome as a set of integral regulatory actors; the final ethylene-mediated plant response is a result of plant and associated microbiota, which collectively forms a holobiont. This association may have large evolutionary implications, in which plants are dependent on their microbiome for adaptive ethylene-mediated responses.