A Legume Genetic Framework Controls Infection of Nodules by Symbiotic and Endophytic Bacteria

Abstract

Legumes have an intrinsic capacity to accommodate both symbiotic and endophytic bacteria within root nodules. For the symbionts, a complex genetic mechanism that allows mutual recognition and plant infection has emerged from genetic studies under axenic conditions. In contrast, little is known about the mechanisms controlling the endophytic infection. Here we investigate the contribution of both the host and the symbiotic microbe to endophyte infection and development of mixed colonised nodules in Lotus japonicus. We found that infection threads initiated by Mesorhizobium loti, the natural symbiont of Lotus, can selectively guide endophytic bacteria towards nodule primordia, where competent strains multiply and colonise the nodule together with the nitrogen-fixing symbiotic partner. Further co-inoculation studies with the competent coloniser, Rhizobium mesosinicum strain KAW12, show that endophytic nodule infection depends on functional and efficient M. loti-driven Nod factor signalling. KAW12 exopolysaccharide (EPS) enabled endophyte nodule infection whilst compatible M. loti EPS restricted it. Analysis of plant mutants that control different stages of the symbiotic infection showed that both symbiont and endophyte accommodation within nodules is under host genetic control. This demonstrates that when legume plants are exposed to complex communities they selectively regulate access and accommodation of bacteria occupying this specialized environmental niche, the root nodule.

Nonnodulating Bradyrhizobium spp. Modulate the Benefits of Legume-Rhizobium Mutualism

“…Our results from clonal inoculations corroborate the results from previous work, which found no effect of nonnodulating strains on legume host growth in isolation (14,25,45). However, under parameters that model relative abundances of nonnodulating strains within the rhizosphere, our data set revealed substantial costs to host growth and symbiont fitness in both host populations examined (except for total nodule biomass at BMR) ( Fig.…”

“…Rhizobia are increasingly being understood to have multifarious lifestyles, including root-nodule symbiosis, colonization of plant roots in the rhizosphere or as root endophytes, and independent growth in the soil or other habitats (24)(25)(26)(27)(28)32). Yet, these lifestyles can be transient and are only partially dependent on the presence or absence of symbiosis loci, which have been a major focus of research.…”

“…Nodulating strains with the canonical nodulation loci, for instance, are not capable of forming nodules on all hosts (e.g., host specificity) (14,43,44). Furthermore, nonnodulating strains (lacking key nodulation genes) can coinfect legume nodules, expropriating a symbiotic role (24,25). Regardless of what factors determine lifestyle, strains that do not form nodules comprise the majority of rhizobial populations that have been sampled (10)(11)(12)(13)(14)(15)(16)(17)(18).…”

“…The proportion of coinfected nodules was increased in strain pairs that were more closely related (0 SNPs) (Table 1), compared to strain pairs that were more distantly related (Ͼ10 SNPs) ( Table 1). One possible explanation for this result is that the similarity of critical signaling molecules during root colonization is more important than abundance for nonnodulating strains (e.g., exopolysaccharides [EPS]) (25). Recently Zgadzaj and colleagues (25) found symbiotic rhizobia with compatible EPS had an advantage over coinfecting endophytes with different EPS molecules.…”

“…More specifically, the relative frequency of nonnodulating versus nodulating rhizobia also varies, but nonnodulating genotypes typically dominate and can encompass as much as 99% of the total rhizobial population (10)(11)(12)(13)(14)(15)(16)(17)(18). Nonnodulating strains can reduce the number of nodules formed by nodulating strains on legume hosts (22,23) and can invade nodule tissues in the presence of closely related nodulating strains (24,25). This suggests that they may be able to reduce nodulating strain fitness through competitive exclusion at the root surface.…”