The Symbiosome: Legume and Rhizobia Co-evolution toward a Nitrogen-Fixing Organelle?

Abstract

In legume nodules, symbiosomes containing endosymbiotic rhizobial bacteria act as temporary plant organelles that are responsible for nitrogen fixation, these bacteria develop mutual metabolic dependence with the host legume. In most legumes, the rhizobia infect post-mitotic cells that have lost their ability to divide, although in some nodules cells do maintain their mitotic capacity after infection. Here, we review what is currently known about legume symbiosomes from an evolutionary and developmental perspective, and in the context of the different interactions between diazotroph bacteria and eukaryotes. As a result, it can be concluded that the symbiosome possesses organelle-like characteristics due to its metabolic behavior, the composite origin and differentiation of its membrane, the retargeting of host cell proteins, the control of microsymbiont proliferation and differentiation by the host legume, and the cytoskeletal dynamics and symbiosome segregation during the division of rhizobia-infected cells. Different degrees of symbiosome evolution can be defined, specifically in relation to rhizobial infection and to the different types of nodule. Thus, our current understanding of the symbiosome suggests that it might be considered a nitrogen-fixing link in organelle evolution and that the distinct types of legume symbiosomes could represent different evolutionary stages toward the generation of a nitrogen-fixing organelle.

Keywords: endosymbiosis; legumes; lupin; nitrogen fixation; nodule; organelle evolution; rhizobia; symbiosome.

Figure 1

Infected cells of legume nodules. (A) Young infected cells showing few symbiosomes and vacuole disintegration; Medicago sativa nodule. (B,C) Symbiosomes in young infected cells; M. sativa (B) and Lupinus albus (C) nodules. Note the dividing symbiosomes (arrowheads). (D) Mature infected cells harboring mature symbiosomes; M. sativa nodule. Low temperature-scanning electron microscopy image (A,D). Transmission electron microscopy image (B,C). b, Bacteroid; cw, cell wall; m, mitochondria; s, symbiosome; sm, symbiosome membrane; v, vacuole.

Figure 2

Nodule of Lupinus albus showing dividing infected cells. (A) Scheme of a nodule section and (B) light microscopy image showing the outer cortex, and the lateral meristematic zone (LMZ) composed of infected and uninfected dividing cells, as well as the central zone composed of infected cells. (C) Detail of the LZM in which the arrows label the symbiosomes. Note the symmetric distribution of symbiosomes between daughter cells. Images (B,C) modified from Fedorova et al. (2005); they are being reproduced with permission from the copyright holder.

Figure 3

Confocal laser images of dividing infected cells of Lupinus albus nodules showing the cytoskeletal elements in green, and the DNA of bacteroids (arrow) and chromosomes (arrowhead) in magenta. (A–D) Metaphase, microtubules (A,B) and actin microfilaments (D). (E) Different anaphase–telophase stages showing the actin microfilaments. n, Nuclei. Images modified from Fedorova et al. (2007); they are being reproduced with permission from the copyright holder.

Figure 4

Scheme for the evolution of different legume nodules and major steps in the nodulation. The characteristics of some legume clades regarding nodulation are shown. D (determinate nodule); I (indeterminate nodule); IC (nodule containing interstitial cells); NIC (nodule lacking interstitial cells); LR (nodule associated with lateral roots); A (aeschynomenoid nodule); LN (lupinoid nodule, only for Lupinus); Des-U (desmodoid nodule exporting ureide); Des-A (desmodoid nodule exporting amide). It was adapted from Sprent and James (2007) and Oono et al. (2010).