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The plant hormone ethylene is one of the central regulators of plant development and stress resistance. Optimal ethylene signaling is essential for plant fitness and is under strong selection pressure. Plants upregulate ethylene production in response to stress, and this hormone triggers defense mechanisms. Due to the pleiotropic effects of ethylene, adjusting stress responses to maximize resistance, while minimizing costs, is a central determinant of plant fitness. Ethylene signaling is influenced by the plant-associated microbiome. We therefore argue that the regulation, physiology, and evolution of the ethylene signaling can best be viewed as the interactive result of plant genotype and associated microbiota. In this article, we summarize the current knowledge on ethylene signaling and recapitulate the multiple ways microorganisms interfere with it. We present ethylene signaling as a model system for holobiont-level evolution of plant phenotype: this cascade is tractable, extremely well studied from both a plant and a microbial perspective, and regulates fundamental components of plant life history. We finally discuss the potential impacts of ethylene modulation microorganisms on plant ecology and evolution. We assert that ethylene signaling cannot be fully appreciated without considering microbiota as integral regulatory actors, and we more generally suggest that plant ecophysiology and evolution can only be fully understood in the light of plant-microbiome interactions.

Growth–defense tradeoffs are a major constraint on plant evolution. While the genetics of resource allocation is well established, the regulatory role of plant-associated microorganisms is still unclear. Here, we demonstrate that plant-associated microorganisms can reposition the plant phenotype along the same growth–defense tradeoff that determines phenotypic effects of plant mutations. We grew plants with microorganisms altering ethylene balance, a key hormone regulating plant investment into growth and stress tolerance. Microbial ethylene reduction had a similar effect to mutations disrupting ethylene signaling: both increased plant growth but at the cost of a strong stress hypersensitivity. We conclude that microbial impact on phenotype can offset the effects of mutations and that apparent plant growth promotion has strong pleiotropic effects. This study confirms that plant life history should be addressed as a joint product of plant genotype and its associated microbiota.

Heavy metal contamination is a threat to global food safety. Reducing heavy metal uptake in plants is a promising way to make plants safer, yet breeding the right set of traits can be tedious. We test whether microorganisms are able to impact the plant’s hormonal balance hereby helping to manage plant heavy metal uptake. We focus on ethylene, a plant hormone regulating plant stress tolerance and nutrition. We grew three phylogenetically distinct plants, Rumex palustris, Alcea aucheri and Arabidopsis thaliana, on a cadmium-spiked soil. Plants roots were coated with the bacterium Pseudomonas putida UW4, which degrades the precursor of ethylene, or an isogenic ACC deaminase-deficient mutant lacking this ability. We followed ethylene concentrations, plant growth and cadmium uptake. Wildtype bacteria reduced shoot cadmium concentration by up to 35% compared to the control, while the mutant increased cadmium concentration. This effect was linked to ethylene, which was consistently positively correlated with cadmium concentration. We therefore propose that bacteria modulating plant hormonal balance may offer new possibilities to improve specific aspects of plant phenotype, in the present context reducing heavy metal. They may thus pave the way for new strategies to improve food safety in a context of the widespread soil contamination.

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.