Resource and Competitive Dynamics Shape the Benefits of Public Goods Cooperation in a Plant Pathogen

Abstract

Cooperative benefits depend on a variety of ecological factors. Many cooperative bacteria increase the population size of their groups by making a public good available. Increased local population size can alleviate the constraints of kin competition on the evolution of cooperation by enhancing the between-group fitness of cooperators. The cooperative pathogenesis of Agrobacterium tumefaciens causes infected plants to exude opines-resources that provide a nearly exclusive source of nutrient for the pathogen. We experimentally demonstrate that opines provide cooperative A. tumefaciens cells a within-group fitness advantage over saprophytic agrobacteria.Our results are congruent with a resource-consumer competition model, which predicts that cooperative, virulent agrobacteria are at a competitive disadvantage when opines are unavailable, but have an advantage when opines are available at sufficient levels. This model also predicts that freeloading agrobacteria that catabolize opines but cannot infect plants competitively displace the cooperative pathogen from all environments. However, we show that these cooperative public goods also promote increased local population size. A model built from the Price Equation shows that this effect on group size can contribute to the persistence of cooperative pathogenesis despite inherent kin competition for the benefits of pathogenesis.

A cooperative virulence plasmid imposes a high fitness cost under conditions that induce pathogenesis

“…The Ti plasmid is able to colonize new agrobacterial genetic backgrounds via conjugative transfer of the plasmid; however, under our experimental conditions, the Ti plasmid conjugal machinery is not expressed-and therefore does not contribute to the plasmid associated costs that we observed. The conjugation of the Ti plasmid is highly regulated such that it only occurs in the disease environment where opines are abundant [16] and in which pTi þ cells have a competitive advantage [42].…”

“…The fitness costs that we have demonstrated in this study probably factor into the observation that the majority of natural agrobacterial isolates lack a virulence-conferring Ti plasmid [43,44], despite the plasmid's high stability [21], ability to conjugate into novel backgrounds [16], and benefits associated with phenolic resistance [45] and opine catabolism [42].…”

“…The costs (figures 2 and 5) and benefits [42] associated with the A. tumefaciens Ti plasmid, as with other plasmids, are environmentally context-dependent. Consequently, the outcome of competition between pTi þ and pTi 2 agrobacteria varies with the environmental conditions in which they are competing.…”

“…This genotype-by-genotype-by-environment interaction Cost of cooperative virulence plasmid T. G. Platt et al 1697 suggests that the Ti plasmid may be subject to selective pressures that vary over space and time. Because of the benefits of opine catabolism, disease environments are likely to be sources for pathogenic agrobacteria [42]. In contrast, non-disease environments are predicted to be sinks for virulent agrobacteria owing to Ti-plasmid-associated costs when resources are limiting.…”

Characterization and phylogenetic diversity of Allorhizobium vitis isolated from grapevine in Morocco

“…; Platt et al . ). Such tumours may also have been caused by atypical agrobacteria, such as narrow host range strains (Knauf et al .…”