Connecting signals and benefits through partner choice in plant–microbe interactions

Abstract

Stabilizing mechanisms in plant-microbe symbioses are critical to maintaining beneficial functions, with two main classes: host sanctions and partner choice. Sanctions are currently presumed to be more effective and widespread, based on the idea that microbes rapidly evolve cheating while retaining signals matching cooperative strains. However, hosts that effectively discriminate among a pool of compatible symbionts would gain a significant fitness advantage. Using the well-characterized legume-rhizobium symbiosis as a model for these general principles, we evaluate the evidence for partner choice in the context of the growing field of genomics. Empirical studies, which rely upon bacteria that only vary in nitrogen-fixation ability, ignore host-symbiont signaling and frequently conclude that partner choice is not a robust stabilizing mechanism. Here, we argue that partner choice is an overlooked mechanism of mutualism stability and emphasize that plants need not use the microbial services provided a priori to discriminate among suitable partners. Additionally, we include a model which shows that partner choice signaling increases symbiont and host fitness in the absence of sanctions. Finally, we call for a renewed focus on elucidating the signaling mechanisms that are critical to partner choice while further aiming to understand their evolutionary dynamics in nature.

Genetic Variation in Host-Specific Competitiveness of the Symbiont Rhizobium leguminosarum Symbiovar viciae

“…This study addressed the question of partner choice at a population level, when multiple compatible host-symbiont associations are possible. In natural soil conditions, the presence of multiple compatible symbiont strains for a given host is generally the rule rather than the exception ( Checcucci et al, 2017 ; Ji et al, 2017 ; Irisarri et al, 2019 ; Younginger and Friesen, 2019 ). In such conditions, the partner choice cannot be simply deduced from the capacities of individual partners but must be analyzed in the context of competition between the various potential associations.…”

“…The host specificity of symbiosis is generally the result of Early Partner Choice ( Younginger and Friesen, 2019 ; Walker et al, 2020 ). EPC is associated with the diversity of the horizontally transferred symbiosis-related regions of the genome, present on specific plasmids or islands ( Young, 2016 ).…”

Experimental Evolution of Legume Symbionts: What Have We Learnt?

“…Following their accommodation into plant cells and when oxygen concentration is low enough, rhizobia initiate nitrogen fixation, the critical process required for nutrient exchanges during this mutualistic symbiosis. a number of studies have shown that nitrogen fixation is not selected at the root entry/nodulation level per se [60,[130][131][132], unless it is associated with another trait [133][134][135]. Instead, post-infection control mechanisms promote fitness of fixing bacteria over non-fixing ones [61,62].…”

Partners in space: Discordant population structure between legume hosts and rhizobium symbionts in their native range

“…For antagonistic interactions, which are governed by negative frequency-dependent selection due to interspecific conflict, models suggest that the partner with a higher migration rate will benefit from the influx of new, potentially adaptive alleles that provide a competitive edge (Gandon et al 1996b;Carlsson-Granér and Thrall 2015). If conflict prevails in mutualisms, and increases in rhizobium fitness occur at the expense of the host (Porter and Simms 2014;Gano-Cohen et al 2020), incongruent population structures between hosts and symbionts should make it harder for hosts to evolve mechanisms to exclude lower-quality symbionts (e.g., partner choice; Akçay 2017;Younginger and Friesen 2019), though this depends on the strength of selection. On the other hand, alignment between host and symbiont fitness might be common in mutualisms, as suggested by recent lab and experimental evolution studies (Friesen 2012;Batstone et al 2020).…”