Microbiota-root-shoot-environment axis and stress tolerance in plants

Reminiscent to the microbiota-gut-brain axis described in animals, recent advances indicate that plants can take advantage of belowground microbial commensals to orchestrate aboveground stress responses. Integration of plant responses to microbial cues belowground and environmental cues aboveground emerges as a mechanism that promotes stress tolerance in plants. Using recent examples obtained from reductionist and community-level approaches, we discuss the extent to which perception of aboveground biotic and abiotic stresses can cascade along the shoot–root axis to sculpt root microbiota assembly and modulate the growth of root commensals that bolster aboveground stress tolerance. We propose that host modulation of microbiota-root-shoot circuits contributes to phenotypic plasticity and decision-making in plants, thereby promoting adaptation to rapidly changing environmental conditions.

Introduction

Belowground and aboveground plant organs are constantly exposed to a number of biotic and abiotic stresses that can change or rapidly fluctuate over time. Because roots and leaves are exposed to different environmental cues, each compartment has evolved organ-specific mechanisms that ensure efficient responses to cognate belowground and aboveground environmental constraints. However, several examples also illustrate that root and shoot organs can ectopically control response to stresses in distant leaves and root compartments, respectively, via long distance communication along the root–shoot axis [1]. For instance, it has been shown that the shoot-derived mobile signal CEPD-like 2 regulates root nitrate uptake according to shoot nitrate status in Arabidopsis thaliana [2] or that shoot-to-root translocation of the mobile transcription factor HY5 mediates light-activated promotion of lateral root growth and nitrogen uptake in A. thaliana [3]. Remarkably, legumes can control nodulation via shoot-to-root translocation of miR2111, a systemic symbiosis activator constitutively repressing nodulation in uninfected roots and ensuring susceptibility to rhizobia in infected roots [4^••]. Finally, root-to-shoot upward migration of cytokinin was shown to act as a signal molecule orchestrating photosynthetic activity in tomato leaves [5]. These selected examples suggest that long distance communication between root and shoot organs are likely key in coordinating growth and development of these two distinct yet interdependent organs, thereby promoting stress tolerance and ensuring plant survival in nature.

Complex multi-kingdom microbial communities have interacted with roots of healthy plants since 450 MyA (i.e., hereafter named the root microbiota [6,7]). Root microbiota members confer numerous beneficial functions to the host linked to nutrient acquisition, pathogen protection or immune system modulation [8, 9, 10, 11, 12, 13, 14, 15,16^••,17, 18, 19]). Given the well-known interplay between the host, the associated microbiota and the environment, it is conceivable that direct integration of responses to microbial commensals belowground and responses to environments aboveground contribute to shoot phenotypic plasticity and aboveground stress resistance in plants. In animals, such long-distance bidirectional communication mechanisms have been extensively described in the context of the microbiota–gut–brain axis [20]. Gut microbiota members were found to modulate mood, cerebral metabolism and behaviour in model gnotobiotic mice systems by 1) modulating the host immune system and immune homeostasis, 2) by impacting the host metabolism (hormones, neuropeptides, neurotransmitters) and 3) by directly interfering with neuronal signalling [20]. In turn, these modifications in brain processes have consequences on gut microbiota assembly, thereby shaping microbiota–gut–brain circuits [20]. Given that plant roots and animal guts share similar physiological functions [21], that the growth of root and shoot organs is tightly coordinated, and that root microbiota members modulate growth and immunity processes in plants, such bidirectional microbiota–root–shoot mechanisms likely play crucial functions for plant health as well [16^••,22^••,23].

In this article, we discuss the extent to which aboveground stresses can modulate root microbiota assembly and conversely how root commensals can mitigate aboveground stress responses (Figure 1). We especially discuss the concept of the microbiota-root-shoot-environment axis in the context of herbivores, microbial leaf pathogens and light stresses because these biotic and abiotic stimuli are specifically perceived by leaves and the consequences on root metabolism and root microbiota assemblages can only be explained by long-distance shoot–root signalling. Using numerous examples obtained from manipulation or microbiota reconstitution experiments, we provide several lines of evidence suggesting that 1) bi-directional communication mechanisms along the microbiota–root–shoot axis promote aboveground stress tolerance 2) selective, host-driven recruitment of particular root commensals acts as a feedback loop that bolsters stress tolerance 3) signals from belowground microbial commensals and aboveground environment are integrated along the microbiota-root-shoot axis to prioritize growth or defence according to the stresses encountered.