Evolutionary history shapes patterns of mutualistic benefit in Acacia –rhizobial interactions

Abstract

The ecological and evolutionary factors that drive the emergence and maintenance of variation in mutualistic benefit (i.e., the benefits provided by one partner to another) in mutualistic symbioses are not well understood. In this study, we evaluated the role that host and symbiont phylogeny might play in determining patterns of mutualistic benefit for interactions among nine species of Acacia and 31 strains of nitrogen-fixing rhizobial bacteria. Using phylogenetic comparative methods we compared patterns of variation in mutualistic benefit (host response to inoculation) to rhizobial phylogenies constructed from housekeeping and symbiosis genes; and a multigene host phylogeny. We found widespread genotype-by-genotype variation in patterns of plant growth. A relatively large component of this variation (21-28%) was strongly influenced by the interacting evolutionary histories of both partners, such that phylogenetically similar host species had similar growth responses when inoculated with phylogenetically similar rhizobia. We also found a relatively large nonphylogenetic effect for the average mutualistic benefit provided by rhizobia to plants, such that phylogenetic relatedness did not predict the overall benefit provided by rhizobia across all hosts. We conclude that phylogenetic relatedness should frequently predict patterns of mutualistic benefit in acacia-rhizobial mutualistic interactions; but that some mutualistic traits also evolve independently of the phylogenies.

Matching population diversity of rhizobial nodA and legume NFR5 genes in plant–microbe symbiosis

“…These genotypes are probably responsible for increased topological similarity between plant and nodule rhizobia gene pools, so that a nodule population is selected by the host plant to supply some needs of the latter. In other words, our results demonstrated the transformation of the initial soil nod A pool by the template of the host plant receptor pool, and this conclusion is in line with the numerous works studying the interplay between diversities of host plant and rhizobia (Andronov et al, ; Bailly, Olivieri, Mita, Cleyt‐Marel, & Bena, ; Barrett, Zee, Bever, Miller, & Thrall, ; Bena, Lyet, Huguet, & Olivieri, ; Depret & Laguerre, ; Österman et al, ; Paffetti et al, ; Rangin, Brunel, Cleyt‐Marel, Perrineau, & Gilles, ; Vuong, Thrall, & Barrett, ). Finally, there are some suggestions on the molecular mechanism involved in this process.…”

Symbiosis limits establishment of legumes outside their native range at a global scale

“…Transplant trials have shown that many legumes rely on soils that are pre-inoculated with compatible microbial symbionts to establish2829 and that soils are highly variable in the abundance303132 and inter-continental genetic structure33 of compatible rhizobia. However, symbiotic nitrogen-fixation has also been implicated in facilitating the invasion of some of the most widespread and problematic legume species of the world30, giving the appearance that compatible rhizobia are cosmopolitan in their distribution.…”

Host species and environmental variation can influence rhizobial community composition

“…; Bever, Broadhurst & Thrall ; Barrett et al . ). To grow and prepare the plants for inoculation, we used a method previously described by Barrett, Broadhurst & Thrall () & Barrett et al .…”

“…a poor strain) (Barrett et al . ). Single strain inoculations provide useful experimental data on variation in host specificity and symbiotic effectiveness, but are limited in terms of addressing questions relating to community dynamics.…”

“…In this study, we used host performance (above‐ground biomass) as a proxy for defining strain effectiveness (Thrall, Burdon & Woods ; Barrett et al . ), such that the more the host grows in response to inoculation with a rhizobial strain, the more effective the strain. Under single strain inoculations, strains can be highly effective and highly specific (specialist), highly effective with low specificity (in this case, a generalist), or have low effectiveness and low specificity (i.e.…”