Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation

• Published in: The New phytologist Vol. 187; no. 2; pp. 508 - 520
• Main Authors: Oono, Ryoko, Schmitt, Imke, Sprent, Janet I., Denison, R. Ford
• Format: Journal Article
• Language: English
• Published: Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01.07.2010; Blackwell Publishing; Blackwell Publishing Ltd; Wiley Subscription Services, Inc
• Subjects: ancestral character state reconstruction; Bacteria; bacteroid; Bacteroids; Bayesian analysis; Biological taxonomies; Differentiation; Electron micrographs; Evolution; Evolution, Molecular; Fabaceae - genetics; Fabaceae - microbiology; Flow Cytometry; Legumes; Life history; Morphology; nodule type; Nodules; Origins; papilionoid legumes; Papilionoideae; Phylogeny; Plants; Probability theory; Quantitative Trait, Heritable; rhizobia; Rhizobium - cytology; Rhizobium - physiology; Root Nodules, Plant - genetics; Root Nodules, Plant - microbiology; Species Specificity; Swelling; Symbiosis; Viability
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/j.1469-8137.2010.03261.x

When rhizobia differentiate inside legume host nodules to become nitrogen-fixing bacteroids, they undergo a physiological as well as a morphological transformation. These transformations are more extreme in some legume species than others, leading to fundamental differences in rhizobial life history and evolution. Here, we analysed the distribution of different bacteroid morphologies over a legume phylogeny to understand the evolutionary history of this host-influenced differentiation. Using existing electron micrographs and new flow cytometric analyses, bacteroid morphologies were categorized as swollen or nonswollen for 40 legume species in the subfamily Papilionoideae. Maximum likelihood and Bayesian frameworks were used to reconstruct ancestral states at the bases of all major subclades within the papilionoids. Extreme bacteroid differentiation leading to swelling was found in five out of the six major papilionoid subclades. The inferred ancestral state for the Papilionoideae was hosting nonswollen bacteroids, indicating at least five independent origins of host traits leading to swollen bacteroids. Repeated evolution of host traits causing bacteroid swelling indicates a possible fitness benefit to the plant. Furthermore, as bacteroid swelling is often correlated with loss of reproductive viability, the evolution of bacteroid cooperation or cheating strategies could be fundamentally different between the two bacteroid morphologies.