Jesús Montiel, J. Allan Downie, Attila Farkas, Péter Bihari, Róbert Herczeg, Balázs Bálint, Peter Mergaert, Attila Kereszt, and Éva Kondorosi

Significance

The mutualistic association between legumes and rhizobia has ecological and agronomical relevance because of its contribution to the global nitrogen cycle by biological nitrogen fixation. Legumes from the Inverted Repeat Lacking Clade (IRLC) impose irreversible differentiation to their endosymbionts through nodule-specific cysteine-rich (NCR) peptides. This study indicates that NCR gene families evolved via different pathways in IRLC species, in which their size and composition directly impacted the morphotype of their bacterial partners. The positive correlation between the diversity of NCRs with their physiological effects on bacteria provides a better understanding of the multiple roles played by this large family in nodule functioning.

Abstract

In legume nodules, rhizobia differentiate into nitrogen-fixing forms called bacteroids, which are enclosed by a plant membrane in an organelle-like structure called the symbiosome. In the Inverted Repeat-Lacking Clade (IRLC) of legumes, this differentiation is terminal due to irreversible loss of cell division ability and is associated with genome amplification and different morphologies of the bacteroids that can be swollen, elongated, spherical, and elongated–branched, depending on the host plant. In Medicago truncatula, this process is orchestrated by nodule-specific cysteine-rich peptides (NCRs) delivered into developing bacteroids. Here, we identified the predicted NCR proteins in 10 legumes representing different subclades of the IRLC with distinct bacteroid morphotypes. Analysis of their expression and predicted sequences establishes correlations between the composition of the NCR family and the morphotypes of bacteroids. Although NCRs have a single origin, their evolution has followed different routes in individual lineages, and enrichment and diversification of cationic peptides has resulted in the ability to impose major morphological changes on the endosymbionts. The wide range of effects provoked by NCRs such as cell enlargement, membrane alterations and permeabilization, and biofilm and vesicle formation is dependent on the amino acid composition and charge of the peptides. These effects are strongly influenced by the rhizobial surface polysaccharides that affect NCR-induced differentiation and survival of rhizobia in nodule cells.

See: http://www.pnas.org/content/114/19/5041.abstract.html?etoc

PNAS May 9 2017; vol.114; no.19: 5041–5046

Fig. 1.  Numbers of NCR peptides in different IRLC legumes are correlated with bacteroid morphology. Numbers of NCR peptides predicted from nodule transcriptomes or genome sequences of 10 IRLC legumes are shown in relation to the morphotype of the bacteroids (A). There is a positive correlation between average bacteroid length and the size of the NCR family (B). Pearson correlation coefficient: 0.90 (P value > 0.001).